bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Phenotypic plasticity triggers rapid morphological convergence
1
2
3
José M. Gómez1,2*, Adela González-Megías2,3*, Eduardo Narbona4*, Luis Navarro5*, Francisco
4
Perfectti2,6*, Cristina Armas1*
5
6
7
1Estación
Experimental de Zonas Áridas (EEZA-CSIC), Almería, Spain.
8
2Research
9
3Dpto.
de Zoología, Universidad de Granada, Granada, Spain.
10
4Dpto.
de Biología Molecular e Ingeniería Bioquímica, Universidad Pablo de Olavide, Sevilla,
11
Spain.
12
5Dpto.
de Biología Vegetal y Ciencias del Suelo, Universidad de Vigo, Vigo, Spain.
13
6Dpto.
de Genética, Universidad de Granada, Granada, Spain.
Unit Modeling Nature, Universidad de Granada, Granada, Spain.
14
15
*Corresponding author. Email: jmgreyes@eeza.csic. (J.M.G.); adelagm@ugr.es (A.G.);
16
enarfer@upo.es (E.N.); lnavarro@uvigo.es (L.N.); fperfect@ugr.es (F.P.); cris@eeza.csic.es
17
(C.A.)
18
1
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
19
Abstract
20
Phenotypic convergence, the independent evolution of similar traits, is ubiquitous in nature,
21
happening at all levels of biological organizations and in most kinds of living beings. Uncovering
22
its mechanisms remains a fundamental goal in biology. Evolutionary theory considers that
23
convergence emerges through independent genetic changes selected over long periods of time.
24
We show in this study that convergence can also arise through phenotypic plasticity. We illustrate
25
this idea by investigating how plasticity drives Moricandia arvensis, a mustard species displaying
26
within-individual polyphenism in flowers, across the morphological space of the entire
27
Brassicaceae family. By compiling the multidimensional floral phenotype, the phylogenetic
28
relationships, and the pollination niche of over 3000 Brassicaceae species, we demonstrated that
29
Moricandia arvensis exhibits a plastic-mediated within-individual floral disparity greater than that
30
found not only between species but also between higher taxonomical levels such as genera and
31
tribes. As a consequence of this divergence, M. arvensis moves outside the morphospace region
32
occupied by its ancestors and close relatives, crosses into a new region where it encounters a
33
different pollination niche and converges phenotypically with distant Brassicaceae lineages. Our
34
study suggests that, by inducing phenotypes that explore simultaneously different regions of the
35
morphological space, plasticity triggers rapid phenotypic convergence.
36
37
2
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
38
Introduction
39
40
Phenotypic convergence, the independent evolution of similar traits in different evolutionary
41
lineages, is ubiquitous in nature, happening at all levels of biological organizations and in most
42
kinds of living beings (1-3). Convergent evolution plays a fundamental role in how evolutionary
43
lineages occupy the morphological space (2, 4). The expansion of lineages across the
44
morphological space is a complex process resulting from the ecological opportunities emerging
45
when species enter into different regions of the ecospace and face new ecological niches (5, 6).
46
When this occurs, divergent selection on some phenotypes makes lineages to diversify
47
phenotypically, boosting morphological disparity, triggering a morphological radiation and
48
eventually filling the morphospace (7, 8). Because the ecological space saturate as lineages
49
diversify (9), unoccupied regions become rare in highly diversified lineages (10). Under these
50
circumstances, entering into a new region usually entails sharing it with other species exploiting
51
the same ecological niche (2, 10, 11). In this situation, independent lineages tend to evolve
52
similar phenotypes through convergent evolution (2, 4). In diversified lineages occupying a
53
saturated morphospace, divergent and convergent evolution are ineludibly connected (10, 12),
54
and both processes contribute significantly to shape the geometry of the morphospace
55
occupation (4, 11).
56
57
Uncovering the mechanisms triggering convergence remains a fundamental goal in biology.
58
Evolutionary theory shows that convergent phenotypes emerge from several genetic
59
mechanisms, such as independent mutations or gene reuse in different populations or species,
60
polymorphic alleles, parallel gene duplication, introgression or whole-genome duplications, that
61
are selected over long periods of time (13–15). Under these circumstances, the origin of
62
morphological convergence is mostly slow, occurring over evolutionary time and associated with
63
multiple events of speciation and cladogenesis (11). It is increasingly acknowledged, however,
64
that phenotypic plasticity might elicit the emergence of novel phenotypes with new adaptive
65
possibilities, which may be beneficial in some contexts (16, 17). Under these circumstances,
66
plasticity may behave as a facilitator for evolutionary novelty and diversity, shaping the patterns of
67
morphospace occupation (16, 18-21). In this study, we provide compelling evidence showing that
68
phenotypic plasticity also plays a prominent role in the emergence of convergent phenotypes. By
69
inducing the production of several phenotypes, plasticity may cause the species to explore
70
different regions of the morphospace almost simultaneously (18, 19). This opens the opportunity
71
for plastic species to diverge from their lineages and converge with the species already located in
72
other morphospace regions. We illustrate this idea by investigating how plasticity drives
73
Moricandia arvensis, a species exhibiting extreme polyphenism in flowers (18), across the
3
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
74
morphological space of the entire Brassicaceae family. Moricandia arvensis displays within-
75
individual floral plasticity, with flower morphs varying seasonally on the same individual (18). By
76
studying the multidimensional floral phenotypes, the phylogenetic relationships, and the
77
pollination niches of over 3000 Brassicaceae species, we demonstrate that phenotypic plasticity
78
makes the flowers of this mustard species to diverge from its ancestors and close relatives, to
79
cross into a new region of the ecospace, and to converge morphologically with distant
80
Brassicaceae lineages. This finding has great implications, suggesting that plasticity might not
81
only promote the evolution of novelties and morphological divergence (16, 17, 20, 21) but can
82
also provide an alternative explanation to the pervasiveness of convergence in nature.
83
84
85
Results
86
87
Plasticity-mediated floral disparity and divergence
88
Changes in temperature, radiation and water availability induce the production of different types
89
of flowers by the same M. arvensis individuals; large, cross-shaped lilac flowers in spring but
90
small, rounded, white flowers in summer (18). To quantify the magnitude of floral disparity
91
between these two phenotypes of M. arvensis, we first assessed floral disparity for the entire
92
mustard family. Brassicaceae is one of the largest angiosperm families, with almost 4000 species
93
grouped in 351 genera and 51 tribes (7, 22–24). We determined the magnitude and extent of
94
floral disparity among 3140 plant species (approx. 80% of the accepted species) belonging to 330
95
genera (94% of the genera) from the 51 tribes. Because we were interested in floral characters
96
mediating the interaction with pollinators, we recorded for each studied species a total of 31 traits
97
associated with pollination in Brassicaceae (Supplementary Data 1, Methods). We used the
98
resulting phenotypic matrix to generate a family-wide floral morphospace. We first run a principal
99
coordinate analysis (PCoA) to obtain a low-dimensional Euclidean representation of the
100
multidimensional phenotypic similarity existing among the Brassicaceae species (25). Because
101
the raw matrix was composed of quantitative, semi-quantitative and discrete variables, PCoA was
102
based on Gower dissimilarities (25). We optimized this initial Euclidean configuration by running a
103
non-metric multidimensional scaling (NMDS) algorithm with 5000 random starts (25). The
104
resulting morphospace (Figure 1a) was significantly correlated with the initial PCoA configuration
105
(r = 0.40, P < 0.0001, Mantel test) and was a good representation of the original relationship
106
among the species (R2 > 0.95, Stress = 0.2, Figure 1b). The distribution of the species across the
107
morphospace was significantly associated with different pollination traits (Figure S1; Table S1).
108
Species in the central region were mostly medium-sized plants bearing a moderate to high
109
number of small, polysymmetric white flowers with short corolla tubes, exposed nectaries and
4
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
110
visible sepals (Figure 1a, Figure S1). Species in the bottom right corner were small or prostrate,
111
bearing minute flowers, many time apetalous and with just 2 or 4 stamens, whereas species
112
located in the bottom left corner were medium-sized plants with asymmetric flowers arranged in
113
corymbous inflorescences. Plants with yellow flowers were located in the right region of the
114
morphospace. In contrast, large plants with strongly tetradynamous androceum and large,
115
veined, dissymmetrical to asymmetrical, pink to blue flowers with concealed nectaries, long
116
corolla tubes and bullseyes were located in the upper left region (Figure 1a, Figure S1).
117
Moricandia arvensis, when blooming in spring (Figure 1c), occupies this later peripheral region of
118
the morphospace, close to other Moricandia species (purple dots in Figure 1a). However, during
119
summertime, the individuals of M. arvensis are shorter and produce fewer, much smaller flowers
120
with white, unveined and rounded corollas with overlapped petals and green sepals that are
121
mostly arranged alone the floral stems (Figure 1d) (18). Due to this radical phenotypic change,
122
the summer phenotype of M. arvensis was located in a different, more central position of the floral
123
morphospace (Figure 1a), far away from the region occupied by the Moricandia species. As a
124
consequence of this jump, the morphological disparity between the spring and summer
125
phenotypes of M. arvensis, calculated as their distance in the morphospace (26), was very high
126
(0.264). In fact, it was much higher than the average pairwise disparities among all studied
127
Brassicaceae species (0.155 ± 0.090, mean ± s.e.m., 4,912,545 pairwise disparities) and almost
128
50% of the largest observed disparity (0.55) (Table S4). This outcome suggests that phenotypic
129
plasticity prompts M. arvensis to explore two distant regions of the Brassicaceae floral
130
morphospace simultaneously.
131
132
To know how intense is the plasticity-mediated M. arvensis disparity, we compared its value with
133
the disparity values observed at different taxonomic levels within Brassicaceae. At the lowest
134
level, discrete changes in pollination traits have been reported between individuals of the same
135
species. In some species, this intraspecific phenotypic change is stable, like the gender
136
polymorphism (27, 28) or the adaptive floral colour polymorphism exhibited as a response to the
137
selective pressures exerted by certain pollinators (29, 30). In other species, discrete phenotypic
138
changes, although affecting pollination traits, seem to be just the consequence of some singular
139
and often unstable mutations affecting floral colour (31), the production of cleistogamous flowers
140
(32) or changes in the expression of homeotic genes that modify the formation of the floral organs
141
(33, 34). We compiled information on the phenotypes of the different morphs in 34 polymorphic
142
species and calculated their values of intraspecific disparities (Figure 1a, Supplementary Data 2).
143
Although several polymorphic species showed considerable values of between-morph disparity,
144
they were significantly smaller than the disparity between spring and summer floral phenotypes of
145
M. arvensis (Z-score = 5.06, P < 0.0001, Figure 1e, Table S2). We subsequently tested at what
5
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
146
taxonomic level of Brassicaceae the disparity was equivalent to the plasticity-mediated disparity
147
observed in M. arvensis. For this, we calculated the floral disparity between pair of species
148
belonging to the genus Moricandia, the same genus, the same tribe, and different tribes
149
(Methods). The plasticity-mediated disparity of M. arvensis was significantly higher than the
150
disparity existing between the Moricandia species (0.057 ± 0.033, mean ± 1 s.e.m., Z-score =
151
6.27, P < 0.0001) and between the species belonging to the same genus (0.069 ± 0.055, Z-score
152
= 3.51, P < 0.0002). It was marginally different from the disparity existing between species of
153
different genera but the same tribes (0.150 ± 0.085, Z-score = 1.34, P = 0.089) and it was
154
statistically similar to the disparity occurring between species belonging to different tribes (0.167 ±
155
0.087, Z-score = 1.11, P = 0.133, Figure 1e). These findings suggest that phenotypic plasticity
156
allows M. arvensis individuals to jump in the morphospace longer distances than those granted
157
by some macroevolutionary processes.
158
159
We explored whether plasticity-mediated disparity may cause evolutionary divergence by
160
calculating the disparity of M. arvensis spring and summer phenotypes to their phylogenetic
161
ancestors. We retrieved 80 partial phylogenies from the literature and online repositories
162
(Methods), and assembled them into a supertree comprising 1876 taxa with information on their
163
floral phenotype. We then projected this supertree onto the morphospace to get a family-wide
164
phylomorphospace. We did not find evidence of phylogenetic constraints on morphospace
165
occupation since there was not significant phylogenetic signal for the position occupied by each
166
species (Multivariate Mantel test=0.005, P = 0.34). The family-wide phylomorphospace was very
167
tangled (Figure 2a), with 492,751 intersections among lineages, suggesting the presence of many
168
events of floral divergence and convergence in the evolution of Brassicaceae pollination traits
169
(11). To calculate the disparity of the M. arvensis floral phenotypes to their ancestor, because
170
these analyses are sensitive to the tree topology and the inferred branch lengths (26), we used
171
four independent, time-calibrated phylogenies that included this species (Methods). The results
172
were consistent across phylogenies (Figure 2b,c; Tables S3). The spring phenotype did not
173
significantly diverge neither from the most recent common ancestor (MRCA) of Moricandia (Z-
174
score = 0.36, P = 0.36) nor from its direct ancestor (Z-score = -1.24, P = 0.108). In contrast, the
175
summer phenotype of M. arvensis diverged significantly both from Moricandia MRCA (Z-score =
176
2.48, P = 0.007) and from its direct ancestor (Z-score = 1.77, P = 0.038). Hence, the summer
177
phenotype explores a region of the floral morphospace located out of its phylogenetic clade range
178
(Figure 2b). The ancestral disparity of the summer phenotype was even significantly higher than
179
the ancestral disparity of most other Brassicaceae species (Figure 2c). These findings suggest
180
that phenotypic plasticity causes the appearance of a novel phenotype that diverges radically
181
from its ancestors.
6
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
182
183
Plastic shifts in pollination niches
184
Evolutionary divergence is mostly associated with the occupation of new ecological niches (2, 5).
185
Shifts between pollination niches are an important factor driving diversification in angiosperms
186
(35), including Brassicaceae (36, 37). We investigated whether the plasticity-mediated jump of M.
187
arvensis across the floral morphospace implicated the exploration of new pollination niches. We
188
compiled a comprehensive database comprising 456,031 visits done by over 800 animal species
189
from 19 taxonomical orders, 276 families and 43 functional groups to 554 Brassicaceae species
190
of 39 tribes (Methods, Supplementary Data 3). Afterwards, we identified the pollination niches of
191
these Brassicaceae plants and determined the niche of each M. arvensis floral phenotype by
192
means of bipartite modularity, a complex network tool that identifies the set of plants interacting
193
with similar groups of pollinators (18). This analysis showed that the network was significantly
194
modular (Modularity = 0.385, P < 0.0001) and identified eight different pollination niches
195
associated with different groups of pollinators (Figure 3a) located in different regions of the
196
morphospace (Figure 3b, F = 44.4, P < 0.001, R2 = 0.39, Adonis test; Table S4).
197
198
Because different insects visited M. arvensis in spring and summer (Table S5), this plant species
199
shifted between pollination niches seasonally (Figure 3b). During spring, M. arvensis belonged to
200
a niche where most frequent pollinators were long-tongued bees, beeflies, and hawkmoths
201
(pollination niche 5 in Figure 3a) (18). This pollination niche was also shared by the other
202
Moricandia species (Figure 3c). In contrast, during summer M. arvensis belonged to a niche
203
dominated by short-tongued bees (pollination niche 3 in Figure 3a). This niche shift was
204
substantial. In fact, the overlap between the spring and summer pollinator niches of M. arvensis
205
(Czekanowski overlap index = 0.35) was significantly lower than the overlap between congeneric
206
species of Brassicaceae (0.57 ± 0.42, Z-score = -0.51, P = 0.003). This shift even entailed the
207
divergence from the ancestral niche of the Moricandia lineage (pollination niche 5 according to a
208
stochastic character mapping inference, Figure 3c). The within-individual floral plasticity allows M.
209
arvensis to exploit a pollination niche that differs markedly from that exploited by its closest
210
relatives and that have largely diverged from the ancestral niche.
211
212
Plasticity-mediated floral convergence
213
A common consequence of adaptation to the same niche is convergent evolution (1, 2, 4). We
214
explored the possibility of convergent evolution of M. arvensis with other Brassicaceae sharing
215
either the spring niche (pollination niche 5) or the summer niche (pollination niche 3). We first
216
checked for the occurrence of convergence among species belonging to these pollination niches.
217
Because these analyses are extremely sensitive to the inferred branch lengths, we explored
7
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
218
morphological convergence using three time-calibrated large (> 150 spp) phylogenies that
219
included M. arvensis (Methods). We tested for the occurrence of floral convergence between the
220
species belonging to each of those two pollination niches using three methods: the angle formed
221
by the phenotypic vectors connecting the position in the floral morphospace of each pair of
222
species with that of their most recent common ancestor (38), the difference in phenotypic
223
distances between convergent species and the maximum distances between all other lineages
224
(39), and the phenotypic similarity of the allegedly convergent species penalized by their
225
phylogenetic distance (Wheatsheaf index) (40). The three methods gave similar results, indicating
226
that floral convergence was frequent among the species belonging to any of the two studied
227
niches, irrespective of the method and the time-calibrated tree used (Table S6). These results
228
show that, despite the rampant generalization observed in the pollination system of Brassicaceae,
229
species interacting with similar pollinators converge phenotypically.
230
231
Once we determined the occurrence of convergence in these two pollination niches, we assessed
232
whether plasticity caused the evolution of morphological convergence in M. arvensis. To do so,
233
we first assessed the convergence region of Moricandia, the region that includes the lineages
234
converging morphologically to the Moricandia lineage. We found that this region included most
235
species of Moricandia, the spring phenotype of M. arvensis, and several clades belonging to
236
disparate tribes that interact with pollination niche 5, but excluded the summer phenotype of M.
237
arvensis (Figure 4, Table S7). Afterwards, we checked whether any of the two M. arvensis floral
238
phenotypes entered the region of the phylomorphospace defined by their pollination niches. We
239
used the C5 index, defined as the number of lineages that cross into the morphospace region of
240
interest from outside39. This index detected between two and six convergent events towards
241
pollination niche 5 depending on the phylogeny used (blue arrows in Figure 4a-c), but none was
242
associated with the spring phenotype of M. arvensis. In contrast, the C5 index consistently
243
detected that the summer phenotype of M. arvensis has converged with the species belonging to
244
the pollination niche 3 (red arrow in Figure 4d-f). Altogether, these analyses suggest that,
245
whereas the spring phenotype did not show any evidence of convergence, the summer
246
phenotype of M. arvensis has converged with other distant Brassicaceae exploiting the same
247
pollination niche.
248
249
250
Conclusions
251
252
Convergent selection exerted by efficient pollinators causes the evolution of similar suites of floral
253
traits in different plant species (41–44). Our study shows that plasticity can promote the rapid
8
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
254
convergent evolution of floral traits, providing an additional explanation about how pollination
255
syndromes may evolve. Under this idea, changes in floral traits precede shifts in pollinators, as
256
frequently observed in generalist systems (37, 45). This may explain why many pollination
257
systems are evolutionarily labile, undergoing frequent shifts and evolve multiple times within the
258
same lineages by diverse evolutionary pathways (35, 46).
259
260
Morphological convergence is universally acknowledged to be the result of several genetic
261
mechanisms, such as independent mutations in different populations or species, polymorphic
262
genes or introgression (13). We provide in this study compelling evidence suggesting that
263
morphological convergence may also arise as a consequence of phenotypic plasticity. The role of
264
plasticity as a mechanism favouring quick responses of organisms to novel and rapidly changing
265
environments is already beyond doubt (17, 21, 47, 48). Its evolutionary consequences are more
266
debated though (20, 21, 49, 50). The ‘plasticity-led evolution’ hypothesis states that selection
267
acting on a plastic lineage may either boost its environmental sensitivity and trigger the origin of
268
polyphenisms or alternatively may promote the loss of plasticity and the canalization of the new
269
phenotype through genetic assimilation (21, 49). The related ‘flexible stem’ hypothesis of adaptive
270
radiation suggests that when a plastic lineage repeatedly colonizes similar niches, the multiple
271
phenotypes fixed by genetic assimilation could converge among them giving rise to a collection of
272
phylogenetically related convergent morphs (16, 50, 51). Our comprehensive study complements
273
these hypotheses by suggesting that plasticity-mediated convergence may even evolve without
274
the existence of basal flexible lineages. Rather, it can occur when plasticity evolving in otherwise
275
non-plastic lineages promotes the colonization of a niche previously occupied by unrelated
276
species. Under these circumstances, contrary to what it is predicted by the previous hypotheses,
277
plasticity-mediated convergence is not circumscribed to phylogenetic-related species arising from
278
a common stem lineage. This overlooked role of phenotypic plasticity may contribute to explain
279
the ubiquity of morphological convergence in nature.
280
281
282
Materials and Methods
283
284
Floral traits. We recorded from the literature 31 floral traits in 3140 Brassicaceae plant species
285
belonging to 330 genera and 51 tribes (Supplementary Data 1). All these traits have been proven
286
to be important for the interaction with pollinators (Table S8). These traits were: (1) Plant height;
287
(2) Flower display size; (3) Inflorescence architecture; (4) Presence of apetalous flowers; (5)
288
Number of symmetry axes of the corolla; (6) Orientation of dominant symmetry axis of the corolla;
289
(7) Corolla with overlapped petals; (8) Corolla with multilobed petals; (9) Corolla with visible
9
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
290
sepals; (10) Petal length; (11) Sepal length; (12) Asymmetric petals; (13) Petal limb length; (14)
291
Length of long stamens; (15) Length of short stamens; (16) Stamen dimorphism; (17)
292
Tetradynamous condition; (18) Visible anthers; (19) Exserted stamens; (20) Number of stamens;
293
(21) Concealed nectaries; (22) Petal carotenoids; (23) Petal anthocyanins; (24) Presence of
294
bullseyes; (25) Presence of veins in the petals; (26) Coloured sepals; (27) Relative attractiveness
295
of petals versus sepals; (28) Petal hue; (29) Petal colour as b CIELAB; (30) Sepal hue; (31) Sepal
296
colour as b CIELAB. A detailed definition and description of these traits and their states is
297
provided in Key Resource Table 1, whereas the original references used to determine the states
298
of each trait per plant species is provided in Supplementary Data 1.
299
300
Family-wide floral morphospace. Using the original multidimensional trait-species matrix, we
301
built a floral morphospace. For this, we reduced the high-dimensional matrix of floral traits to a
302
two-dimensional space using an ordination technique (25). Because the set of floral traits
303
included in this study were quantitative, semi-quantitative and qualitative, we used ordination
304
techniques based on dissimilarity values. For this, we first constructed a pairwise square distance
305
matrix of length equal to the number of Brassicaceae species included in the analysis (n = 3140).
306
We used the Gower distance, the number of mismatched traits over the number of shared traits.
307
This dissimilarity index is preferable to the raw Euclidean distance when there are discrete and
308
continuous traits co-occurring in the same dataset (52).
309
We reduced the dimensionality of this phenotypic matrix by projecting it in a two-dimensional
310
space. For this, to ensure an accurate description of the distribution of the species in the
311
morphospace, we first run a principal coordinate analysis (PCoA), a technique providing a
312
Euclidean representation of a set of objects whose relationship is measured by any dissimilarity
313
index. We corrected for negative eigenvalues using the Cailliez procedure (25). Afterwards, we
314
used this metric configuration as the initial configuration to run a non-metric multidimensional
315
scaling (NMDS) algorithm (25), a method that will further optimise the sample distribution so as
316
more variation in species composition is represented by fewer ordination axes. Unlike methods
317
that attempt to maximise the variance or correspondence between objects in an ordination,
318
NMDS attempts to represent, as closely as possible, the pairwise dissimilarity between objects in
319
a low-dimensional space. NMDS is a rank-based approach, where the original distance data is
320
substituted with ranks, preserving the ordering relationships among species (25). Objects that are
321
ordinated closer to one another are likely to be more similar than those further apart (53). This
322
method is more robust than distance-based methods when the original matrix includes variables
323
of contrasting nature. However, NMDS is an iterative algorithm that can fail to find the optimal
324
solution. We decreased the potential effect of falling in local optima by running the analysis with
325
5000 random starts and iterating each run 1 x 106 times (54). The NMDS was run using a
10
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
326
monotone regression minimizing the Kruskal's stress-1 (55, 56), and compared each solution
327
using Procrustes analysis, retaining that with the lowest residual. Because many species did not
328
share trait states, a condition complicating ordination, we used stepacross dissimilarities, a
329
function that replaces dissimilarities with shortest paths stepping across intermediate sites while
330
regarding dissimilarities above a threshold as missing data (57). Furthermore, we used weak tie
331
treatment, allowing equal observed dissimilarities to have different fitted values. The scores of the
332
species in the final ordination configuration were obtained using weighted averaging. We checked
333
if the reduction in dimensionality maintained the between-species relationship by checking the
334
stress of the resulting ordination and finding goodness of fit measure for points in nonmetric
335
multidimensional scaling (54). Both PCoA and NMDS ordinations were done using the R package
336
vegan (58) and ecodist (59). It is important to note that, although the transfer function from
337
observed dissimilarities to ordination distances is non-metric, the resulting NMDS configuration is
338
Euclidean and rotation-invariant (60).
339
340
Morphological Disparity. Because we were interested in describing the position of the species
341
in the floral morphospace, we calculated the morphological disparity using indices related to the
342
distance between elements (26, 61). We first determined the absolute position of each of the
343
Brassicaceae species in the morphospace by calculated their Euclidean distance with the overall
344
centroid of the morphospace (61). The disparity between the spring and summer phenotype of M.
345
arvensis was also calculated as their Euclidean distance in the floral morphospace. We then
346
calculated the pairwise disparities between all species included in our analysis, between the
347
different morphs of the polymorphic species considered here (Supplementary Data 2), between
348
the species of the genus Moricandia, between species of the same genus, between species of
349
different genera but same tribe and between species of different tribes. These disparity values
350
were calculated using the function dispRity of the R package dispRity using the command
351
centroid (62). We checked whether the disparity between spring and summer M. arvensis
352
phenotypes was significantly different from the disparities of each of these sets of species using
353
Z-score tests.
354
355
Family-wide phylogeny. We retrieved 80 phylogenetic trees from the literature and from the
356
online repositories TreeBase (Table S9). All trees were downloaded in nexus format. The
357
taxonomy of the species included in each tree was checked and updated using the species
358
checklist with accepted names provided by Brassibase (https://brassibase.cos.uni-heidelberg.de/)
359
(7, 23, 63). All trees were converted to TreeMan format (64) and concatenated into a single
360
TreeMen file that was then converted into a multiPhylo class. Afterward, we estimated a
361
supertree from this set of trees. Because trees did not share the same taxa, we used the Matrix
11
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
362
representation parsimony method (65). To make this supertree more accurate, it was re-
363
constructed using as backbone phylogeny the tree provided by Walden et al. (7). We removed
364
from the supertree those species without information on floral phenotype, resulting in a tree with
365
1876 taxa. Because the original trees used to assemble this supertree where very
366
heterogeneous, this supertree was not dated. We finally rooted the supertree using several
367
species belonging to the sister families Capparaceae and Cleomaceae (66). All phylogenetic
368
manipulations were performed using the R libraries treebase (67), ape (68), treeman (64),
369
phangorn (69) and phytools (70).
370
We tested whether the position of the Brassicaceae species in the morphospace was
371
associated with the phylogenetic relationship by assessing the phylogenetic signal of the
372
morphospace position. This analysis was performed by means of a multivariate Mantel test, using
373
the pairwise disparity (the Euclidean distance between species in the family-wide morphospace)
374
as a morphological distance and the patristic distances between pairs of tips of the supertree as
375
the phylogenetic distance (71). The correlation method used was Pearson and the statistical
376
significance was found after bootstrapping 999 times the analysis (25). The test was done using
377
the R libraries vegan (58) and ecodist (59).
378
379
Family-wide phylomorphospace. We reconstructed a family-wide phylomorphospace by
380
projecting the phylogenetic relationships provided by the supertree into the floral morphospace.
381
The ancestral character estimation of morphospace coordinate values for each internal tree node
382
was done using maximum likelihood. For this, we used the function fastAnc in phytools. This
383
function performs fast estimations of the ML ancestral states for continuous traits by re-rooting
384
the tree at all internal nodes and computing the contrasts state at the root each time (70).
385
We counted the number of intersections between lineages as a measurement of the
386
disorder of the phylomorphospace and evidence of the mode of evolution of the phenotypes (11).
387
For this, we used R codes provided in Ref 11. We compared the observed number of crossings
388
with those expected under several modes of evolution. For this, we counted the number of
389
intersections in 10 simulated sets of species with floral phenotypes following Brownian Motion,
390
Ornstein Uhlenbeck and Early Burst modes of evolution. All simulations were done using as
391
backbone tree the family-wide supertree and considering 1875 species, and by means of the
392
command mvSIM in mvMORPH (72).
393
394
Morphological divergence of the plastic phenotypes. Divergence in floral phenotype was
395
estimated by calculating the disparity of Moricandia arvensis and the rest of Brassicaceae
396
species from their ancestors. We first determined the floral phenotype of the Most Recent
397
Common Ancestor (MRCA) using the projection of a recent time-calibrated phylogeny made for
12
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
398
the genus Moricandia (73) into the above-described phylomorphospace. We used this phylogeny
399
because it is the only one including all the species of the genus. Once we inferred the coordinates
400
of the MRCA in the morphospace, we calculated the disparity of all the Moricandia species and
401
the two plastic phenotypes of M. arvensis to it. Afterwards, we calculated the divergence of the
402
two plastic phenotypes from the direct ancestor of M. arvensis. This analysis was done for the
403
family-wide supertree and for any of the four time-calibrated phylogenies included in our dataset
404
that had Moricandia species (73-76). In addition, we calculated the divergence from the direct
405
ancestors of the rest of Brassicaceae species included in these four phylogenies and in the rest
406
of the time-calibrated trees included in our dataset (Table S9). All floral divergences were
407
calculated using the command ancestral.dist of the function dispRity in the R package dispRity
408
(62).
409
410
Pollinator Database. We have compiled a massive database including 21,212 records
411
comprising 455,014 visits done by over 800 animal species from 19 taxonomical orders, 276
412
families and 43 functional groups to 554 Brassicaceae species belonging to 39 tribes
413
(Supplementary Data 3). Information is coming from literature, personal observation, online
414
repositories and personal communication of several colleagues. The source of information is
415
indicated in the database (Supplementary Data 3, Table S10). In those species studied by us
416
(coded as UNIGEN data origin in the Supplementary Data 3), we conducted flower visitor counts
417
in 1-16 populations per plant species. We visited the populations during the blooming peak,
418
always at the same phenological stage and between 11:00 am and 5:00 pm. In these visits, we
419
recorded the insects visiting the flowers for two hours without differentiating between individual
420
plants. Insects were identified in the field, and some specimens were captured for further
421
identification in the laboratory. We only recorded those insects contacting anthers or stigma and
422
doing legitimate visits at least during part of their foraging at flowers. We did not record those
423
insects only eating petals or thieving nectar without doing any legitimate visit. The information
424
obtained from the literature and online repositories (coded as LITERATURE data origin in the
425
Supplementary Data 3) includes records done during ecological studies, taxonomical studies and
426
naturalistic studies. The reference of every record is included in the dataset. The plant species
427
included in our network do not coexist, implying that this is a clade-oriented network rather than
428
an ecological network (77).
429
430
Spatial distribution of pollinator groups. We tested the autocorrelation across the
431
morphospace in the abundance of the functional groups using a multivariate Mantel test. The
432
correlation method used was Pearson, and the statistical significance was found after
433
bootstrapping 999 times the analysis (25). The test was done using the R libraries vegan (58).
13
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
434
435
Pollination niches. In plant species interacting with a diverse assemblage of pollinators, like
436
those included in this study, many pollinator species interact with the flowers in a similar manner,
437
have similar effectiveness and exert similar selective pressures and are thus indistinguishable for
438
the plant (46, 78). These pollinators are thus grouped into functional groups, which are the
439
relevant interaction units in generalised systems (46, 78, 79). We thereby grouped all pollinators
440
visiting the Brassicaceae species using criteria of similarity in body length, proboscis length,
441
morphological match with the flower, foraging behaviour, and feeding habits (46, 78, 79). Table
442
S11 describes the 43 functional groups used in this study. Supplementary Data 4 shows the
443
species with an autogamous pollination system.
444
445
We determined the occurrence of different pollination niches in our studied populations and
446
seasons using bipartite modularity, a complex-network metric. Modularity has proven to be a
447
good proxy of interaction niches both in ecological networks, those included coexisting species or
448
population, as well as in clade-oriented network, those including species with information coming
449
from disparate and contrasting sources (77). We constructed a weighted bipartite network,
450
including pollinator data of four populations during the spring and summer flowering. In this
451
network, we pooled the data from the different individuals in a population and did not consider the
452
time difference involved in sampling across different species. We removed all plant species with
453
less than 20 visits. We subsequently determined the modularity level in this weighted bipartite
454
network by using the QuanBiMo algorithm (80). This method uses a Simulated Annealing Monte-
455
Carlo approach to find the best division of populations into modules. A maximum of 1010 MCMC
456
steps with a tolerance level = 10-10 was used in 100 iterations, retaining the iterations with the
457
highest likelihood value as the optimal modular configuration. We tested whether our network was
458
significantly more modular than random networks by running the same algorithm in 100 random
459
networks, with the same linkage density as the empirical one (81). Modularity significance was
460
tested for each iteration by comparing the empirical versus the random modularity indices using a
461
Z-score test (80). After testing the modularity of our network, we determined the number of
462
modules (82). We subsequently identified the pollinator functional groups defining each module
463
and the plant species ascribed to each module. Modularity analysis was performed using the R
464
package bipartite 2.0 (83). We quantified the niche overlap between all pair of Brassicaceae
465
species using the Czekanowski index of resource utilization, an index that measures the area of
466
intersection of the resource utilization histograms of each species pair (84). This index was
467
calculated using the function niche.overlap in the R package spaa (85).
468
14
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
469
Estimation of ancestral values of pollination niches. The ancestral states of the pollination
470
niche was inferred for the Moricandia lineage by simulate stochastic character mapping of
471
discrete traits with Bayesian posterior probability distribution (86, 87). Three models of character
472
evolution ("ER" - Equal Rates; “SYM” – symmetric; and “ARD” - All Rates Different) were first
473
evaluated using the fitDiscrete function of the R package Geiger (88). The best model was
474
selected using the Akaike Information Criterion (AIC) and used for stochastic character mapping.
475
The posterior distribution of the transition rate matrix was determined using a Markov chain
476
Monte Carlo (MCMC) simulation, and the stochastic mapping was simulated 100 times.
477
Stochastic character mapping was performed using the make.simmap function and a plot of
478
posterior probabilities were mapped using the describe.simmap function in R package ‘phytools
479
(70).
480
481
Morphological convergence. To explore morphological convergence, we reconstructed the
482
ancestral states of the species belonging to these two pollination niches and tested for each niche
483
whether the species were morphologically more similar to each other than expected by their
484
phylogenetic relationship (39, 40). We used three different approaches to detect morphological
485
convergence, one based on comparing phenotypic and phylogenetic distances (39) and the other
486
based on comparing the angles formed by two tested clades from their most recent common
487
ancestor with the expected angle according to null evolutionary models (38). Because all these
488
analyses are sensitive to the number of tips in the phylogeny and the inferred branch lengths, we
489
tested for the occurrence of morphological convergence using three independent, time-calibrated
490
phylogenies including more than 45 species (74-76).
491
Under the first approach, we calculated both distance- and frequency-based measures of
492
convergence (39). Distance-based measures (C1–C4) are calculated between two lineages
493
relative to their distance at the point in evolutionary history where the two lineages were
494
maximally dissimilar. C1 specifically measures the proportion of phenotypic distance closed by
495
evolution, ranging from 0 to 1 (where 1 indicates complete convergence). To calculate C1,
496
ancestral states are reconstructed (via a Brownian motion model of evolution) for two or more
497
putatively convergent lineages, back to their most recent common ancestor. The maximum
498
phenotypic distance between any pair of ancestors (Dmax) is calculated, and compared with the
499
phenotypic distance between the current putatively convergent taxa (Dtip). The greater the
500
difference between Dmax and Dtip, the higher the index. C2 is the raw value of the difference
501
between the maximum and extant distance between the two lineages. C3 is C2 scaled by the
502
total evolution (sum of squared ancestor-to-descendant changes) between the two lineages. C4
503
is C2 scaled by the total evolution in the whole clade. These four measures quantify incomplete
504
convergence in multidimensional space. Finally, C5, the frequency-based measure, quantifies
15
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
505
and reports the number of convergent events where lineages evolve into a specific region of
506
morphospace (crossing it from outside). C5 sums the number of times through the evolution of a
507
clade that lineages evolve into a given region of phenotypic space. C5 is the number of focal taxa
508
that reside within a limited but convergent region of a phylomorphospace (the phylogenetic
509
connections between taxa represented graphically in a plot of morphological space). The
510
significance of C1–C5 was found by running 1000 simulations for each comparison using
511
Brownian-Motion on a variance–covariance matrix based on data-derived parameters, with
512
convergence measures for each simulation calculated to determine if the observed C value is
513
greater than expected by chance. A priori focal groups forming the basis of convergence tests
514
were the same niche categorizations used in OUwie analyses. These analyses were performed
515
using the R package convevol (89).
516
The second approach to measure convergence was based on comparing the angles
517
formed by two tested clades from their most recent common ancestor with the expected angle
518
according to null evolutionary models (38). Under the “state case”, search.conv computes the
519
mean angle over all possible combinations of species pairs using one species per state. Each
520
individual angle is divided by the patristic distance between the species. Significance is assessed
521
by contrasting this value with a family of 1,000 random angles obtained by shuffling the state
522
across the species (38). These analyses were performed using the R package RRphylo (90).
523
The third approach to measure convergence used the Wheatleaf metric (40). This index
524
generates phenotypic (Euclidean) distances from any number of traits across species and
525
penalizes them by phylogenetic distance before investigating similarity (in order to weight close
526
phenotypic similarity higher for distantly related species). It uses an a priori designation of
527
convergent species, which are defined as species belonging to a niche for which the traits are
528
hypothesized to converge. The method then calculates a ratio of the mean (penalized) distances
529
between all species to the mean (penalized) distances between allegedly convergent species.
530
The index detects if convergent species diverge more in phenotypic space from the non-
531
convergent species and show a tighter clustering to each other (40). The significance of this index
532
was found by comparing the empirical values of the index with a distribution of simulated indices
533
obtained running 5000 bootstrap simulations. These analyses were performed using the R
534
package windex (91).
535
536
537
Acknowledgments
538
Authors thank Raquel Sánchez, Angel Caravantes, Isabel Sánchez Almazo, María José
539
Jorquera, and Iván Rodríguez Arós for helping us during several phases of the study. We also
540
thank all contributors to the pollinator database (Table S10) for kindly sending us unpublished
16
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
541
information on Brassicaceae floral visitors. This research is supported by grants from the Spanish
542
Ministry of Science, Innovation and Universities (CGL2015-63827-P, CGL2017-86626-C2-1-P,
543
CGL2017-86626-C2-2-P, UNGR15-CE-3315), Junta de Andalucía (P18-FR-3641, IE19_238
544
EEZA CSIC), LIFE18 GIE/IT/000755, and Xunta de Galicia (CITACA), including EU FEDER
545
funds. This is a contribution to the Research Unit Modeling Nature, funded by the Consejería de
546
Economía, Conocimiento, Empresas y Universidad, and European Regional Development Fund
547
(ERDF), reference SOMM17/6109/UGR.
548
549
Competing interests
550
The authors declare no competing interests.
551
552
553
References
554
1. G. R. McGhee, Convergent Evolution: Limited Forms Most Beautiful. MIT Press, Cambridge
555
556
557
558
559
560
561
562
563
(2011). ISBN:9780262016421
2. J. B. Losos, Convergence, adaptation, and constraint. Evolution 65, 1827–1840 (2011).
doi:10.1111/j.1558-5646.2011.01289.x
3. S. C. Morris, Life's solution: Inevitable Humans in a Lonely Universe. Cambridge University
Press, Cambridge (2003). ISBN:9780521603256
4. T. Pearce, Convergence and parallelism in evolution: a Neo-Gouldian account. Br. J. Philos.
Sci. 63, 429–448 (2011). doi:10.1093/bjps/axr046
5. D. Schluter, The Ecology of Adaptive Radiation. Oxford Univ. Press, Oxford, U.K. (2000)
ISBN:9780198505228
564
6. P. Nosil, Ecological Speciation. Oxford Univ. Press, Oxford, U.K. (2012) ISBN:9780199587100
565
7. N. Walden, D. A. German, E. M. Wolf, M. Kiefer, P. Rigault, X. C. Huang, C. Kiefer, R.
566
Schmickl, A. Franzke, B. Neuffer, K. Mummenhoff, Nested whole-genome duplications
567
coincide with diversification and high morphological disparity in Brassicaceae. Nature Comm.
568
11, 3795 (2020). doi:10.1038/s41467-020-17605-7
569
8. M. Simões, L. Breitkreuz, M. Alvarado, S. Baca, J. C. Cooper, L. Heins, K. Herzog, B. S.
570
Lieberman, The evolving theory of evolutionary radiations. Trends Ecol. Evol. 31, 27–34
571
(2016). doi:10.1016/j.tree.2015.10.007
572
573
574
575
9. M. R., Pie, J. S. Weitz, A null model of morphospace occupation. Am. Nat. 166, E1–E13
(2005). doi:10.1086/430727
10.K. O. Winemiller, D. B. Fitzgerald, L. M. Bower, E. R. Pianka, Functional traits, convergent
evolution, and periodic tables of niches. Ecol. Lett. 18, 737–751 (2015). doi:10.1111/ele.12462
17
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
576
11.C. T. Stayton, Are our phylomorphospace plots so terribly tangled? An investigation of
577
disorder in data simulated under adaptive and nonadaptive models. Curr. Zool. 66, 565–574
578
(2020). doi:10.1093/cz/zoaa045
579
12.A. L. Pigot, C. Sheard, E. T. Miller, T. P. Bregman, B. G. Freeman, U. Roll, N. Seddon, C. H.
580
Trisos, B. C. Weeks, J. A. Tobias, Macroevolutionary convergence connects morphological
581
form to ecological function in birds. Nature Ecol. Evol. 4, 230–239 (2020).
582
doi:10.1038/s41559-019-1070-4
583
584
585
13.D. L. Stern, The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764
(2013). doi:10.1038/nrg3483
14.E. B. Rosenblum, C. E. Parent, E. E. Brandt, The molecular basis of phenotypic convergence.
586
Annu. Rev. Ecol. Evol. Syst. 45, 203–226 (2014). doi:10.1146/annurev-ecolsys-120213-
587
091851
588
589
590
591
592
593
594
15.P. A. Christin, D. M. Weinreich, G. Besnard, Causes and evolutionary significance of genetic
convergence. Trends Genet. 26, 400–405 (2010). doi:10.1016/j.tig.2010.06.005
16.M. J. West-Eberhard, Developmental Plasticity and Evolution. Oxford Univ. Press, New York,
(2003). ISBN: 9780195122343
17.S. Sultan, Organism and Environment: Ecological development, Niche construction, and
Adaption. Oxford Univ. Press, New York, (2015). ISBN:9780199587063
18.J. M. Gómez, F. Perfectti, C. Armas, E. Narbona, A. González-Megías, L. Navarro, L. DeSoto,
595
R. Torices, Within-individual phenotypic plasticity in flowers fosters pollination niche shift.
596
Nature Comm. 11, 4019 (2020). doi:10.1038/s41467-020-17875-1
597
19.V. Susoy, E. J. Ragsdale, N. Kanzaki, R. J. Sommer, Rapid diversification associated with a
598
macroevolutionary pulse of developmental plasticity, eLife 4, e05463 (2015).
599
doi:10.7554/eLife.05463
600
601
602
603
604
605
606
20.N. A. Levis, D. W. Pfennig, Evaluating ‘plasticity-first ’evolution in nature: key criteria and
empirical approaches. Trends Ecol. Evol. 31, 563–574 (2016). doi:10.1016/j.tree.2016.03.012
21.R. J. Sommer, Phenotypic plasticity: from theory and genetics to current and future
challenges. Genetics 215, 1–13 (2020). doi:10.1534/genetics.120.303163
22.M. A. Koch, D. A. German, M. Kiefer, A. Franzke, Database taxonomics as key to modern
plant biology. Trends Plant Sci. 23, 4–6 (2018). doi:10.1016/j.tplants.2017.10.005
23.M. Kiefer, R. Schmickl, D. A. German, T. Mandáková, M. A. Lysak, I. A. Al-Shehbaz, A.
607
Franzke, K. Mummenhoff, A. Stamatakis, M.A. Koch, BrassiBase: introduction to a novel
608
knowledge database on Brassicaceae evolution. Plant Cell Physiol. 55, e3–e3 (2014).
609
doi:10.1093/pcp/pct158
610
611
24.The Plant List Version 1.1. Published on the Internet (accessed 1st January 2021).
http://www.theplantlist.org/1.1/browse/A/Brassicaceae/ (2013).
18
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
612
25.P. Legendre, L. Legendre, Numerical Ecology. Elsevier, Oxford (2012). ISBN:9780080523170
613
26.T. Guillerme, N. Cooper, S. L. Brusatte, K. E. Davis, A. L. Jackson, S. Gerber, A. Goswami, K.
614
Healy, M. J. Hopkins, M. E. Jones, G. T. Lloyd, Disparities in the analysis of morphological
615
disparity. Biol. Lett. 16, 20200199 (2020). doi:10.1098/rsbl.2020.0199
616
27.M. Méndez, J. M. Gómez, Phenotypic gender in Hormathophylla spinosa (Brassicaceae), a
617
perfect hermaphrodite with tetradynamous flowers, is variable. Plant Syst. Evol. 262, 225–23
618
(2006). doi:10.1007/s00606-006-0462-5
619
28. V. L. Soza, V. Le Huynh, V. S. Di Stilio, Pattern and process in the evolution of the sole
620
dioecious member of Brassicaceae. EvoDevo 5, 42 (2014). doi:10.1186/2041-9139-5-42
621
29.E. Narbona, H. Wang, P. L. Ortiz, M. Arista, E. Imbert, Flower colour polymorphism in the
622
Mediterranean Basin: occurrence, maintenance and implications for speciation. Plant Biol. 20,
623
8–20 (2018). doi:10.1111/plb.12575.
624
30.C. A. Dick, J. Buenrostro, T. Butler, M. L, Carlson, D. J. Kliebenstein, J. B. Whittall, Arctic
625
mustard flower color polymorphism controlled by petal-specific downregulation at the threshold
626
of the anthocyanin biosynthetic pathway. PLoS One 6, e18230 (2011).
627
doi:10.1371/journal.pone.0018230
628
31.B. Zhang, C. Liu, Y. Wang, X. Yao, F. Wang, J. Wu, G. J. King, K. Liu, Disruption of a
629
carotenoid cleavage dioxygenase 4 gene converts flower colour from white to yellow in
630
Brassica species. New Phytol. 206, 1513–1526 (2015). doi:10.1111/nph.13335
631
32.S. Faisal, Y. Guo, S. Zang, B. Cao, G. Qu, S. Hu, Morphological and genetic analysis of a
632
cleistogamous mutant in rapeseed (Brassica napus L.). Genet. Resour. Crop Evol. 65, 397–
633
403 (2018). doi:10.1007/s10722-017-0598-x
634
635
33.G. Theissen, Homeosis of the angiosperm flower: studies on three candidate cases of
saltational evolution. Palaeodiversity 3, 131–139 (2010).
636
34.M. V. Byzova, J. Franken, M. G. Aarts, J. de Almeida-Engler, G. Engler, C. Mariani, M. M. V.
637
L. Campagne, G. C. Angenent, Arabidopsis STERILE APETALA, a multifunctional gene
638
regulating inflorescence, flower, and ovule development. Genes Dev. 13, 1002–1014 (1999).
639
doi:10.1101/gad.13.8.1002.
640
35.T. Van der Niet, S. D. Johnson, Phylogenetic evidence for pollinator-driven diversification of
641
angiosperms. Trends Ecol. Evol. 27, 353–361 (2012). doi:10.1016/j.tree.2012.02.002
642
36.A. Franzke, M. A. Lysak, I. A. Al-Shehbaz, M. A. Koch, K. Mummenhoff, Cabbage family
643
affairs: the evolutionary history of Brassicaceae. Trends Plant Sci. 16, 108–116 (2011).
644
doi:10.1016/j.tplants.2010.11.005
645
646
37.J. M. Gómez, F. Perfectti, J. Lorite, The role of pollinators in floral diversification in a clade of
generalist flowers. Evolution 69, 863–878 (2015). doi:10.1111/evo.12632
19
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
647
38.S. Castiglione, C. Serio, D. Tamagnini, M. Melchionna, A. Mondanaro, M. Di Febbraro, A.
648
Profico, P. Piras, F. Barattolo, P. Raia, A new, fast method to search for morphological
649
convergence with shape data. PloS One 14: e0226949 (2019).
650
doi:10.1371/journal.pone.0226949
651
39.C. T. Stayton, The definition, recognition, and interpretation of convergent evolution, and two
652
new measures for quantifying and assessing the significance of convergence. Evolution 69,
653
2140–2153 (2015). doi:10.1111/evo.12729
654
40.K. Arbuckle, C. M. Bennett, M. P. Speed, A simple measure of the strength of convergent
655
evolution. Methods Ecol. Evol. 5, 685–693 (2014). doi:10.1111/2041-210X.12195
656
41.K. Faegri, L. Van Der Pijl, Principles of Pollination Ecology. Elsevier, Oxford (1980).
657
658
659
660
ISBN:9780080164212
42.A. S. Dellinger, Pollination syndromes in the 21st century: where do we stand and where may
we go?. New Phytol. 228, 1193–1213 (2020). doi:10.1111/nph.16793
43.R. D. Phillips, R. Peakall, T. van der Niet, S. D. Johnson, Niche perspectives on plant–
661
pollinator interactions. Trends Plant Sci. 25, 779–793 (2020).
662
doi:10.1016/j.tplants.2020.03.009.
663
44.C. A. Wessinger, L. C. Hileman, Parallelism in flower evolution and development. Annu. Rev.
664
Ecol. Evol. Syst. 51, 387–408 (2020). doi:10.1146/annurev-ecolsys-011720-124511
665
45.J. D. Thomson, P. Wilson, Explaining evolutionary shifts between bee and hummingbird
666
pollination: convergence, divergence, and directionality. Int. J. Plant Sci. 169, 23–38 (2008).
667
doi:10.1086/523361
668
46.J. M. Gómez, F. Perfectti, M. Abdelaziz, J. Lorite, A. J. Muñoz Pajares, J. Valverde, Evolution
669
of pollination niches in a generalist plant clade. New Phytol. 205, 440–453 (2015).
670
doi:10.1111/nph.13016
671
47.E. C. Snell-Rood, M. E. Kobiela, K. L. Sikkink, A. M. Shepherd, Mechanisms of plastic rescue
672
in novel environments. Annu. Rev. Ecol. Evol. Syst. 49, 331–354 (2018). doi:10.1146/annurev-
673
ecolsys-110617-062622
674
48.R. J. Fox, J. M. Donelson, C. Schunter, T. Ravasi, J. D. Gaitán-Espitia, Beyond buying time:
675
the role of plasticity in phenotypic adaptation to rapid environmental change. Phil. Trans. R.
676
Soc. B 374, 20180174 (2019). doi:10.1098/rstb.2018.0174
677
49.N. A. Levis, D. W. Pfennig, Plasticity-led evolution: evaluating the key prediction of frequency-
678
dependent adaptation. Proc. Biol. Sci. 286, 20182754 (2019). doi:10.1098/rspb.2018.2754
679
50.M. R. Warner, L. Qiu, M. J. Holmes, A. S. Mikheyev, T. A. Linksvayer, Convergent eusocial
680
evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes.
681
Nature Comm. 10, 1–11 (2019). doi:10.1038/s41467-019-10546-w
20
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
682
683
684
685
686
51.R. F. Schneider, A. Meyer, How plasticity, genetic assimilation and cryptic genetic variation
may contribute to adaptive radiations. Mol. Ecol. 26, 330–350 (2017). doi:10.1111/mec.13880
52.T. Guillerme, N. Cooper, Time for a rethink: time sub sampling methods in disparity through
time analyses. Palaeontology 61, 481–493 (2018). doi:10.1111/pala.12364
53.P. Legendre, D. Borcard, P. R. Peres-Neto, Analyzing beta diversity: Partitioning the spatial
687
variation of community composition data. Ecol. Monogr. 75, 435–450 (2005). doi:10.1890/05-
688
0549
689
690
691
692
693
694
54.P. Mair, I. Borg, Rusch T. Goodness-of-fit assessment in multidimensional scaling and
unfolding. Multivar. Behav. Res. 51, 772–789 (2016). doi:10.1080/00273171.2016.1235966.
55.J. B. Kruskal, Multidimensional scaling by optimizing goodness-of-fit to a nonmetric
hypothesis. Psychometrika 29, 1–28 (1964).
56.J. B. Kruskal, Nonmetric multidimensional scaling: a numerical method. Psychometrika 29,
115–129 (1964).
695
57.G. De'ath, Extended dissimilarity: a method of robust estimation of ecological distances from
696
high beta diversity data. Plant Ecol. 144, 191–199 (1999). doi:10.1023/A:1009763730207
697
58.J. Oksanen, F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’hara, G. L.
698
Simpson, P. Solymos, M. H. H. Stevens, H. Wagner, 2013 Package ‘vegan’. Community
699
ecology package, version 2, 1–295 https://cran.r-project.org,
700
https://github.com/vegandevs/vegan (2019)
701
702
703
704
705
59.S. C. Goslee, Urban, D. L The ecodist package for dissimilarity-based analysis of ecological
data. J. Stat. Softw. 22, 1–19 (2007). doi:10.18637/jss.v022.i07
60.J. Oksanen, Vegan: an introduction to ordination. URL http://cran. r-project.
org/web/packages/vegan/vignettes/introvegan.pdf (2020).
61.T. Guillerme, M. N. Puttick, A. E. Marcy, V. Weisbecker, Shifting spaces: Which disparity or
706
dissimilarity measurement best summarize occupancy in multidimensional spaces?. Ecol.
707
Evol. 10, 7261–7275 (2020). doi:10.1002/ece3.6452
708
709
710
62.T. Guillerme, dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9,
1755–1763 (2018). doi:10.1111/2041-210X.13022
63.M. A. Koch, M. Kiefer, D.A. German, I.A. Al-Shehbaz, A. Franzke, K. Mummenhoff, R.
711
Schmickl, BrassiBase: Tools and biological resources to study characters and traits in the
712
Brassicaceae — version 1.1. Taxon 61, 1001–1009 (2012). doi:10.1002/tax.615007
713
64.D. J., Bennett, M. D., Sutton, S. T. Turvey, Treeman: an R package for efficient and intuitive
714
manipulation of phylogenetic trees. BMC Res. Notes 10, 30 (2017). doi:10.1186/s13104-016-
715
2340-8
716
717
65.M. A. Ragan, Phylogenetic inference based on matrix representation of trees. Mol.
Phylogenetics Evol. 1, 53–58 (1992). doi:10.1016/1055-7903(92)90035-F
21
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
718
719
66.S. Bayat, M. E. Schranz, E. H. Roalson, J. C. Hall, Lessons from Cleomaceae, the sister of
crucifers. Trends Plant Sci. 23, 808–821 (2018). doi:10.1016/j.tplants.2018.06.010.
720
67.C. Boettiger, D. Temple Lang, Treebase: an R package for discovery, access and
721
manipulation of online phylogenies. Methods Ecol. Evol. 3, 1060–1066 (2012).
722
doi:10.1111/j.2041-210X.2012.00247.x
723
68.E., Paradis, K. Schliep, ape 5.0: an environment for modern phylogenetics and evolutionary
724
analyses in R. Bioinformatics 35, 526–528 (2019). doi:10.1093/bioinformatics/bty633
725
69.K. Schliep, phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).
726
727
728
doi:10.1093/bioinformatics/btq706
70.L. J. Revell, phytools: an R package for phylogenetic comparative biology (and other things).
Methods Ecol. Evol. 3, 217–223 (2012). doi:10.1111/j.2041-210X.2011.00169.x
729
71.O. J. Hardy, S. Pavoine, Assessing phylogenetic signal with measurement error: a comparison
730
of Mantel tests, Blomberg et al.'s K, and phylogenetic distograms. Evolution 66, 2614–2621
731
(2012). doi:10.1111/j.1558-5646.2012.01623.x
732
72.J. Clavel, G. Escarguel, G. Merceron, mvMORPH: an R package for fitting multivariate
733
evolutionary models to morphometric data. Methods Ecol. Evol. 6, 1311–1319 (2015).
734
doi:10.1111/2041-210X.12420
735
73.F. Perfectti, J. M. Gómez, A. González-Megías, M. Abdelaziz, J. Lorite, Molecular phylogeny
736
and evolutionary history of Moricandia DC (Brassicaceae). PeerJ 5, e3964 (2017).
737
doi:10.7717/peerj.3964
738
739
740
74.S. A. Smith, J. W. Brown, Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot.
105, 302–314 (2018). doi:10.1002/ajb2.1019
75.M. L. Gaynor, J. Ng, R. G. Laport, Phylogenetic structure of plant communities: are polyploids
741
distantly related to co-occurring diploids?. Frontiers Ecol. Evol. 6, 52 (2018).
742
doi:10.3389/fevo.2018.00052
743
76.X.-C. Huang, D. A. German, M. A. Koch, Temporal patterns of diversification in Brassicaceae
744
demonstrate decoupling of rate shifts and mesopolyploidization events. Ann. Bot. 125, 29–47
745
(2019). doi:10.1093/aob/mcz123
746
77.J. M. Gómez, M. Verdú, F. Perfectti, Ecological interactions are evolutionarily conserved
747
across the entire tree of life. Nature 465, 918–921 (2010). doi:10.1038/nature09113
748
78.C. B. Fenster, W. S. Armbruster, P. Wilson, M. R. Dudash, J. D. Thomson, Pollination
749
syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35, 375–403 (2004).
750
doi:10.1146/annurev.ecolsys.34.011802.132347
751
79.J. M. Gómez, R. Torices, J. Lorite, C. P. Klingenberg, F. Perfectti, The role of pollinators in the
752
evolution of corolla shape variation, disparity and integration in a highly diversified plant family
753
with a conserved floral bauplan. Ann. Bot. 117, 889–904 (2016). doi:10.1093/aob/mcv194
22
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
754
755
756
757
758
759
760
761
762
763
764
765
766
767
768
769
770
771
772
773
774
80.C. F. Dormann, R. Strauss, A method for detecting modules in quantitative bipartite networks.
Methods Ecol. Evol. 5, 90–98 (2014). doi:10.1111/2041-210X.12139
81.R. Guimerà, L. A. N. Amaral, Functional cartography of complex metabolic networks. Nature
433, 895–900 (2005). doi:10.1038/nature03288
82.M. E. J. Newman, Analysis of weighted networks. Phys. Rev. E70, 056131 (2004).
doi:10.1103/PhysRevE.70.056131
83.C. F. Dormann, B. Gruber, J. Fründ, Introducing the bipartite package: Analysing ecological
networks. R News 8, 8–11 (2008).
84.P. Feinsinger, E. E. Spears, R. W. Poole, A simple measure of niche breadth. Ecology 62, 27–
32 (1981). doi:10.2307/1936664
85.J. Zhang, M. J. Zhang, Package ‘spaa’. R package version 1. https://CRAN.Rproject.org/package=spaa (2013).
86.J. P. Huelsenbeck, R., Nielsen, J. P. Bollback, Stochastic mapping of morphological
characters. Syst. Biol. 52, 131–158 (2003). doi:10.1080/10635150390192780
87.J. P. Bollback, SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC
Bioinformatics 7, 88 (2006). doi:10.1186/1471-2105-7-88
88.L. J. Harmon, J. T. Weir, C. D. Brock, R. E. Glor, W. Challenger, GEIGER: investigating
evolutionary radiations. Bioinformatics 24, 129–131 (2008). doi:10.1093/bioinformatics/btm538
89.C. T. Stayton, Convevol: quantifies and assesses the significance of convergent evolution. R
package version 1.0. See http:// cran.r-project.org/ web/packages/convevol/index.html (2018).
90.P. Raia, S. Castiglione, C. Serio, A. Mondanaro, M. Melchionna, M. Di Febbraro, RRphylo:
775
Phylogenetic ridge regression methods for comparative studies. Methods Ecol. Evol. 9, 974-
776
983 (2019). doi:10.1111/2041-210X.12954
777
778
91.K., Arbuckle, A. Minter, Windex: Analyzing convergent evolution using the Wheatsheaf index
in R. Evol. Bioinformatics 11, EBO-S20968 (2015). doi:10.4137/EBO.S20968
779
23
b oRx v p ep n do h ps do o g 10 1101 2021 05 25 445642 h s ve s on pos ed May 26 2021 The copy gh ho de o h s p ep n wh ch
was no ce ed by pee ev ew s he au ho unde who has g an ed b oRx v a cense o d sp ay he p ep n n pe pe u y
s made
ava ab e unde aCC BY 4 0 n e na ona cense
780
781
782
Figures
b
d
Hesperis varolii
Micran tha mul ticaulis
Matthiola anchoniifolia
Matthiola iranica
Farsetia longisiliqua
Matthiola valesiaca
Matthiola macranica
Farsetia linearis
Matthiola fruticulosa
Eruca vesicaria
Matthiola flavida
Enarthrocarpus arcuatus
Matthiola chenopodiifolia
0.2
Hesperis syriaca
Matthiola chorassanica
Hesperis tristis
Brassi ca incana
Mach aerop horus matthioloides
Conrin gia grandiflora
Matthiola glutinosa
Eruca pinnatifida
Chorispora iberica
Brassi ca drepanensis
Hesperis balansae
Dithyrea californica
Matthiola shiraziana
Lyroca rpa coulteri
Erysi mum men ziesii
Bra ssica olerace a
Bra ssica macroca rpa
Eutrema baimashanicum
Biscu tella cichoriifolia
Brassi ca trich ocarpa
Hesperis pendula
Coincya longirost ra
Carin avalva glauca
Matthiola arabica
Farsetia assa dii
Erysimum polatschekii
Leavenworthia stylosa
Hesperis stellata
Bra ssica bivoniana
Erysimum macrop etalum
Brassi ca montana
Eutrema renifolium
Coincya rich eri
Hesperis scabrida
Hesperis breviscapa
Coincya monensis.cheiran thos
Hesperis kuerschneri
Coincya transtagana
Brassica raimondoi
Mathewsia foliosa
Brassi ca bourgeaui
Degenia velebitica
Mathewsia peruvi ana
Erysimum f rancisca num
Conrin gia austria ca
Erysi mum p erof ski anum
Erysimum ca pitatum
Erysi mum d agest anicum
Arabis kaynakiae
Brassi ca napus
Erysi mum p seudocheiri
Erysi mum co ncinnum
Leavenworthia texana
Matthiola fragans
Mathewsia linearif olia
Erysimum o sse ticum
Mathewsia densifolia
Draba hammenii
Erysi mum b aicalense
Hesperis campicarpa
Farsetia heliophila
Erysimum su ffrutescens
Erysimum ghiesbreghtii
Erysi mum n ervosu m
Erysimum croce um
Erysi mum g abrie lianae
Erysi mum i bericu m
Erysimum co llinum
Leavenworthia a urea
Hesperis candida
Chorispora macropoda
Alysso ides utricu laria
Bra ssi ca villosa
Coincya rupestris
Erysimum roseum
Conringia planisiliqua
Bra ssi ca tinei
Erysimum w itmanni
Leavenworthia crassa
Farsetia jacquemontii
Erysimum ko tuchovii
Mathewsia collina
Erysi mum mun zurie nse
Erysimum hezarense
Hesperis novakii
Diplotaxis antoniensi s
Coincya monensis.orop hila
Erysimum b onannianum
Erysimum a penninum
Erysimum a ren icola
Erysi mum met lesicsi i
Erysi mum o ccidentale
Erysimum p ignattii
Diplotaxis hirta
Mathewsia auriculata
Atacama nivea
Enarthrocarpus pterocarpus
Leavenworthia torulosa
0.1
Matthiola bucharica
Hesperis tosyaensis
Bra ssi ca maurorum
Hesperis hamzaoglui
Hesperis buschiana
Matthiola integrifolia
Matthiola kralikii
Eruca foleyi
Hesperis bottae
Hesperis pisidica
Aethionema lepidioides
Erysimum semperflorens
Erysimum funiculosum
Erysimum cyaneum
Leiospora beketovii
Hesperis thyrsoidea
Moricandia spinosa
Orychophragmus zhongtiaoshanus
Marcus-kochia lacera
Eremophyton chevallieri
Moricandia nitens
Matthiola capiomontana
Leiospora bellidifolia
Brassica hilarionis
Erysimum pseudopurpureum
Arabis aubrietoides
Erysimum lilacinum
Erysimum purpureum
Hesperis trullata
Leiospora eriocalyx
Parrya minjanensis
Parrya arctica
Hesperis hedgei
Douepia tortuosa
Orychophragmus taibaiensis
Clausia trichosepala
Chorispora purpurascens
Orychophragmus longisiliquus
Parrya nauruaq
Cardamine gouldii
Moricandia sinaica
Foleyola billotii
Cardamine raphanifolia
Erysimum bastetanum
Chorispora bungeana
Orychophragmus violaceus
Clausia aprica
Hesperis sibirica
Marcus-kochia triloba
Cardamine dentata
Malcolmia maritima
Brachypus suffruticosus.kermanshahensis
Erysimum linifolium
Lunaria rediviva
Parolinia plastypetala
Cardamine constancei
Erysimum cazorlense
Hesperis pycnotricha
Farsetia longistyla
Heliophila rimicola
Heliophila filicaulis
Parolinia filifolia
Brachypus suffruticosus.suffruticosa Parolinia glabriuscula
Lunaria annua
Brachypus suffruticosus.khoshyelaqensis
Horwoodia dicksonia
Parrya khorasanica
Erysimum bicolor
Hesperis kitiana
Parolinia
inrtermedia
Erysimum
popovii
Henophyton
zygarrhenum
Moricandia foetida
Arabis blepharophylla
Marcus-kochia arenaria
Boechera formosa
Cardamine pachystigma
Maresia doumetiana
Menonvillea cuneata
Boechera pulchra
Cardamine picta
Cakile maritima
Arabis mollis.mollis
Cardamine concatenata
Heliophila scandens
Cardamine montenegrina
Boechera
fernaldiana
Boechera
Boechera
californica
arcuata
Dontostemon senilis
Cardamine maxima
Arabis mollis.graellsiiformis
Noccaea al-atahanii
Boechera hoffmannii
Dontostemon
dentatuscrassifolius
Dontostemon
Cardaminepratensis
rivularis
Cardamine
Hesperidanthus barnebyi
Arabidospsis cebennensis
Arabis josiae
Maresia pygmaea
Hesperidanthus argillaceus Goldbachia sabulosa
Cardamine angulata
Arabis rosea
Eigia longistyla
Heliophila esterhuyseniae
Cakile constricta
Arabidopsisdelavayi
cebennensis
Dontostemon Megacarpaea
perennis
Heliophila cedarbergensis
Lunaria telekiana
Aubrieta libanotica
Maresia malcolmioides
Phoenicaulis cheiranthoides
Arabis verna
Aethionema
elongatum
Cardamine
purpurea
Aethionema semnanensis
Aubrieta erubescens
Heliophila alpina
Aethionema cordatum
Aubrieta parviflora
Aubrieta ekimii
AethionemaAethionema
thomasianum
schistosum
Notothlaspi rosulatum
-0.1
Heliophila digitata
Heliophila africana
Heliophila arenaria
Heliophila coronopifolia
Iberis nazarita
Heliophila adpressa
Crambe hedgei
Iberis attica
Iberis peyerimhofjii
Cardamine pseudotrifoliolata Crambe sventenii
Crambe feuilleei
Crambe
strigosa
Crambe
laevigata
Crambe
schugnana
Crambe
edentula
Arabis stenocarpa
Crambe
microcarpa
Crambe
tamadabensis
Crambe
steveniana
Crambe koktebelica
Crambe
fruticosa
Crambe
scoparia
Crambe
juncea
Crambe pinnatifida
Crambe
armena
Crambe
scaberrima
Crambe
orientalis
Crambe grossheimii
Crambe Crambe
gomeraealutacea
Noccaea bulbosa
Heliophila amplexicaulis
Iberis ciliata.contracta
Iberis ciliata.welwitschii
Iberis runemarkii
Chamira circaeoides
Phravenia viereckii
Alyssu m w ulfenianum
Isa tis afghanica
Alyssu m mou radicum
Pa ysonia lyrat a
Drab a matthioloidesPh ysariaPhysa
engelmannii
ria alpina
Draba rosi tae
Diplotaxis tenuifolia
Barba rea vulgaris
Diplotaxis muralis
Diplotaxis tenuisiliqua
Isatis apennina
Meniocus st ylaris
Brassi ca procu mbens
Isa tis takhtajanii
Meniocus huetii
Bra ssi ca souliei Diplotaxis assurge ns
Isa tis raimondoi
Alyssu m n ive um
Physa
ria ria
pinetorum
Physa
riapruinosa
ovalifolia
Physa
pendula
Physa
Physa
ria
carin
ata
Payso nia auricu lata
Payso nia lescu rii
Al yssu
m p ersicu
m ria obco rdata
Alyssu mDraba
lepidoto-ste
llatum
sagast
eguii
Physa
Au rin ia petraea
Physa
rollinsi
i
Ph
ysaria
rect
ipes
Physa
riariaintermedia
Physa ria oregona
Physa
ria kingii
Physa
occi dentalis
m rep Bu
ensnias orie ntalis
Physa
riariasaximontana
Draba Alyssu
japonica
Physa
ria
ludoviciana
Physa
calcicola
Physa
ria argyrae a
Physa
riaria
densiflora
Diplotaxis siifolia
Drab a pulvinata Physa ria douglasii
ria parvul a
Physa
ria Physa
arenosa
Physa
ria
Physa
ria angustifolia
cordiformis
Physa
graci lis
Drab
a bifurcat
aria
Brassi ca jordanoffii
Physa
ria calderi
Physa
Physa
ria macroca
ria garre rpa
ttii
ria gooddingii
Payso nia densipila
Diplotaxis catholica
Draba litamo Physa
Physa
ria arizo
fremon
tii
Ph
ysaria
nica
Ph ysariaPhysa
hemiphysaria
Neslia apiculata
Drab a xyl opoda
humilis
Physa
ria lata
Physa
riariareediana
Ph ysaria
prost
rata
Au rinia
sinuata
Physa
ria
Physa
Phria
ysaria
ria nelsonii
gordonii
Physa
hitchco
ckii
Di plotaxis brevi si liqua
Physa
ria condensata
Physa
ria lindheimeri
Physa ria scrot iformi s
Drab a aureo la
Physa ria ria
klausii
arcti ca
navajoensis
Draba pseudocheiran thoidesPh ysariaPhysa
Eruca strum i fniense
Phiaysa
incrassa
taria
Aurin
leucadea
DrabDraba
a rit acu
vana
ysa
ria lesicii
aurea
Draba
kassi
Alyssui m Ph
amasi
anum
Physa ria parvif lora
Physa ria obdeltata
Physa
ria recu rvat a
Physa
ria pachyphylla
Physa
Physa
riaria
cocurvip
ngestaes
Physa ria pycn antha
Draba
wurdackii
Drab a aizoides
Draba
aleutica
Drab
a funcki
ana
globosa
PhPhysa
ysariariapulvinata
Odontarrhena
mughlaei
Draba ruaxes
Eruca strum a byssi nicum
Di plotaxis virgata
Drab a ochrop etala
Alyssu m ca lyco carpum
Kremerie lla cordyl
Alyssuocarpus
m pse udomouradicum
Al yssu m mue lleri
bulbotrich
um
Alyssu m trich
ocarpum
Isatis aucheri
Alyssu m misi rdalianum
Eru castrum ca rdamin oides
Guirao a arven sis
Drab a pamplonensis
ria chambersii
Draba pennell-ha zeniiPhysaPhysa
riariagrahamii
Ph ysa
bellii
Ph ysaria multiceps
Physa
montana
Physa
olia
Drab a funcki
i riaria
Physa
riaintegrif
fendleri
pulcherri ma
Diplotaxis harra Draba
Physa ria erio carpa
Draba sch ultzei
Erysimum i ncanum
ria cinerea
PhysaPhysa
ria floribunda
Drab a co cuyanaPhysa ria newberryi
Eruca strum vi rgatum
Alyssu m hezarmasjedense
Eru cast rum ca narie nse
Aurin ia saxa tilis
Physa
ria didymoca
rpa
Brassi
ca somalensis
Physa
ria dornii
Physa ria brassi coides
Alyssu m p raecox
Eruca strum p alustre
Bra ssi ca deflexa
Iberis grossi
Iberis aurosica.aurosica
Iberis aurosica.nana
Heliophila affinis
Iberis linifolia
Pennellia boliviensis
Heliophila macowaniana
Pennellia patens
Mostacillastrum g raci elae
Exhalimolobos hispidulus
Ianhedgea minutiflora
Isa tis djurdjurae
Isa tis tinctoria
Alyssu m mon tanum
Biscutella incana
Brassi ca tournefortii
Odontarrh ena obovata
Cardamin e basicola
Peltaria alliacea
Ionopsidium albiflorum
Cardamin e rese difolia
Geococcu s pusillus
Cruci himalaya bursif olia
Ara bis pumil a
Arabis lycia
Isa tis erzurumica
Isatis co chlearis
Isatis ca ndolleana
Isa tis kozlowskyi
Isa tis kotschyana
Isatis stenophylla
Isatis cappadocica
Isa tis platyloba
Isa tis florib unda
Clypeola erio carpa
Clypeola elegans
Clypeola ci liata
Clypeola raddeana
Clypeola dichotoma
Lepidium co ronopus
Cardamine bilobata
Lepidium mon tanum
Lepidium juvencum
Lepidium nitidum
Lepidium se ditiosum
Lepidiumcucaneiforme
pitatum
Lepidium
Lepidium
amissu m
Lepidium
crassu m yotum
Lepidium
Lepidium dict
a cutidens
LepidiumLepidium
ca stellanum
oxyca rpum
Heliophila roggeveldensis
Cardamine
Berteroa
obliqua
Cardamine
papilla a tasarif olia
Berte roa mut abilitis
Chlorocrambe hastata
Clypeola jonthlaspi
At hysa nus pusillus
Menkea sphaerocarpa
Lepidium p hlebopetalum
Cardamine pa ucijuga
Ionopsidium abulense
Microt hlaspi sylvarum-ce dri
Noccaea minima
Heliophila ephemera
Exh alimol obos weddellii
Ba llantinia antipoda
Lepidotrich um uechtrit zi anum
Cardamin e corymb osa Bra yopsis gamosepala
Asch erson
Asche
iodoxa
rsonmandoniana
iodoxa pilosa
Brayopsis
Brayo psisdiapensi
colombioides
ana
Didesmus bipinnatus
Didesmus aegyptius
Microt hlaspi mediterraneo-orie ntale
Draba werffii
Crambegigantea
santosii
Crambe
Lepidium gramin ifolium
Lepidium virgi nicum
Heliophila varia bilis
Lepidium desva uxi i
Lepidium f lexicaule
Sphaeroca rdamum n esliiforme
Phyllolepidum
ocarpum
Microt cycl
hlaspi
perfoliatum
Ionopsidium prolongoi
Nocca ea densiflora
Heliophila goldblattii
Pe nnellia yalaensis
Pen nellia brach yca rpa
Didymophysa aucheri
Erophila tenerri na
Lepidium boelcke i
Lepidium ki rkii
Carda mine cubita
Prin glea antiscorbu tica
Lepidium ginninderrense
Pennellia lasiocalycina
Coronopus didymus
Iren epharsus tryph erus
Iberis odorata
Menkea australis
Iberis saxatilis.magnesiana
Carda ria draba
Lepidium bonarie nse
Lepidium d ensiflorum
Heliophila cornuta Onuris alismatifolia
Iberis
carica
Iberis
spruneri
Pennellia longifolia
Isatis violascens
Coronopus lepidioides
Coronopus violaceus
Sp haeroca rdamum macrum
Sphaeroca rdamum st ellatum
Lepidium l eptopetalum
Nocca ea violasce ns
Iberis fontqueri
Onuris
hatcheriana
Onuris
papillosa
Onuris spegazziniana
Coron opus squamatus
Lepidium galapagoensis
Bra yopsis chacasensis
Onuris graminifolia
Callothlaspi lilacinum
Conrin gia clavata
Delpinophytum p atagonicu m
Lepidium su bulatum Lepidium lasi ocarpum
Lepidium latipes
Lepidium oblongum
LepidiumLepidium
ramosi ssi
stmum
rict
um
Lepidium
rud
erale
Lepidium
Lepidiumapetalum
payso
nii
Lepidium
so
rdidum
Lepidium
pereg
rinum
Microt hlaspi
erra ticum
Frie drich karlmeye
ria umbellata
Crambe pritzelii
Crambeaspera
tataria
Crambe
Noccaea stilosa
Heliophila acuminata
Iberis arbuscula
Isa tis spectabilis
Isa tis bitilisica
Isa tis undulata
Isa tis spatella
Isa tis frig ida
Isatis callifera
Isa tis nummularia
Isatis karja ginii
Isatis besse ri
Isa tis Isatis
lockman
niana
arenaria
Isatis brach yca rpa
Idahoa scapigera
Irenepharsus phasmat odes
Crambe hispanica
Iberis spathulata
Iberis simplex
Iberis bernardiana
Isatis pinnatiloba
Isa tis sivasica
Isatis amani
Isatis armena
Al yssu m f lexicaule
Diplotaxis vimin ea
Lepidium p anniforme
Lepidium corda tum
Lepidium ca lyco trich um
Lepidium glastifolium
HeliophilaHeliophila
co rnellsbergia
patens
Heliophila diffusa
Kot sch yella cilici ca
Lepidium ca mpestre
Ero
Ero
phila
phila
min
verna
ima
Lepidium st ron gylophyllum Cardamine trich ocarpa
Ionopsidium sa vianum
Cochlearia sco ticaArab is eriki i
Cardamin e caesiella
Pennellia microsperma
Iberis linifolia.pruitii
Iberis pinnata
Isatis prae cox
Isa tis vermi a
Alyssu m baumgartn eria num
m vo urinonense
Meniocus Alyssu
blepharoca
rpus
Alyssu m lyca onicum
Biscu tella va lentina
Boechera duchesnensis
Cardamine polemonioides
Arab idella glaucesce ns
Cardamine
penduliflora
Crambe
cordifolia
Lachnoloma lehmannii
Boechera
lasiocarpa
Boechera
pratincola
Boechera atrorubens
Boechera
Boechera
davidsonii
cusickii
Boechera
breweri
Arabis ionocalyx
Arabis Arabis
bijuga stelleri
Boechera consanguinea
Boechera
glaucovalvula
Boechera
gracilipes
Boechera
porphyrea
Boechera
shockleyi
Boechera
acutina
Boechera
lyallii
Cakile
maritima
Crambe maritima
Boechera
goodrichii
Boechera
Boechera
drepanoloba
divaricarpa
Boechera
fendleri
Boechera
inyoensis
Boechera
pallidifolia
Boechera
perennans
pauciflora
Boechera
puberula
Boechera
rubicundula
rollinsiorum
rigidissima
Boechera
serpenticola
Boechera
texana
Arabis brachycarpa
Dontostemon pinnatifidus
Dontostemon
pinnatifidus
linearifolius
pinnatifidus
Heliophilaintegrifolius
hurkana
Dontostemon
Heliophila katbergensis
Boechera
gracilenta
Boechera
tularensis
Cakileretrofracta
geniculata
Heliophila elongata
Boechera
calderi
Boechera
harrisonii
Cithareloma lehmannii
Arabis flagellosa
Boechera
howellii
Boechera
falcifructa
falcatoria
Dontostemon micranthusBoechera
Fourraea alpina Cardamine tenera
Arabis turrita
Cardamine calthifolia
Arabis serrata
Cardamine douglassii
Arabis
pterosperma
Cardamine dissectaBoechera
Boechera
horizontalis
hastatula
Boechera
elkoensis
Boechera
peirsonii
Boechera
pinetorum
Boechera
covilleiCakile lanceolata
Boechera
cascadensis
Menonvillea scapigera Arabis furcata
Arabis carduchorum
Arabis
eschscholtziana
Boechera lemmonii
Arabis
deflexa
Galitzkya
spathul ata
Dontostemon glandulosus Boechera
fructicosa
Boechera
gunnisoniana
Boechera
languida
Boechera
Boechera
pendulocarpa
paupercula
pendulina
Boechera
platysperma
Boechera
schistacea
Aplanodes
doidgeana
Eutrema
robustum
Heliophila nubigena
Cardamine
cordifolia
Heliophila monospermaDryopetalon
Boechera multijuga
nevadensis
Cardamine purpurascens
Cardamine
trifida
Cardamine
Cardamine yezoensis
auriculatum
Boechera
glareosa
Boechera
suffrutescens
Arabis
georgiana
Boechera
paddoensis
Boechera
dispar
Physaria pallida
Mostacillastrum sagittatum CardamineBoechera
gracilis
Boechera
Boechera
Boechera
microphylla
oxylobula
macounii
ophira
Boechera
pinzliae
pusilla
saximontana
Boechera
shevockii
Boechera
tiehmii
villosa
Aplanod
es sisymbrio
ides
cobrensis
Cardamin
e prorep
ens
Goldbachia ikonnikovii
Arabis erecta
Nasturtium gambe llii
Eutrema scapiflorum
Boechera
depauperata
Cardamine
fragariifolia
Cardamine
microzyga
Boech era
holboellii
Boeche
ra polyantha
Boechera bodiensis
Boes chera grah amii
Goldbachia verrucosa
Chaunanthus torulosu
Mosta
cillastrum
pcran
urpusii
Cardamine anemonoides
Carda
mine uliginosa
Carda
mine
wiedemanniana
Card
amin
equebecensis
sca
posa
Boe
chera
dallii
Arabi
sra
soyeri
Arabis elgonensis
Dendroarabis fruticulosa
Boeche
Boechera perstellata
Farsetia occidentalis
Neuontobotrys mendocina Card amine californica
Berteroa physocarpa
Draba sanctae-martae
Ara bis nuttallii
Aethionema syriacum
Arabis androsacea
Boech era lignifera
Cardamine schinziana
Boechera spatifolia
Mostacillastrum
st
enophyllum
Aethionema sabzevaricum
Ara bis
grae
llsiiformis
Acirostrum
alaschanicum
Neuontobotrys polyphylla
Cardamine ovata
Mostacillastrum
subauricu
Cardamin
elatum
tuberosa
Cardamine
lilacina
Aethionema froedinii
Menonvillea spathulata
Aethionema anatolicum
Crucihimalaya
wallichii
Cardamine appendiculata
Arabis doumetii
Boechera
stricta
Crucihimalaya
stricta
Aethionema virgatum
Draba bruniifolia
pubens
DrabaMostacill
hederif olia
sagittata
Cardamine
tenuirost
ris eburniflora
astHalimolobos
rumArabis
sul bsca
ndens
Physa
ria
Noccaea aghrica
Aethionema
umbellatum
Alyssu mAlyssu
u mbellatum
Cardamine tangutorum
planisiliqua
Draba
oreadum
eptocarpum
Crucihimalaya
mollissima himalaica
Neuontobotrys frutescens Mostac illastrum Arabis
malysso
st apfiiides
Aethionema
transhyrcanum
Lepidium j aredii
Crucihimalaya
Alyssu m
Heliophila macrosperma
Nerisyrenia camporum
Arabis
glabra
Heliophila schulzii
Most
acillastrum
co m
mmune
Crucihimalaya axilaris
Aubrieta vulcanica
Pach
ycladon
fasci
ariu
Arabis conringioides
Arabis sudetica
Eutrema
verticillatum
echera
constancei
AraBo
bis
amplexicaulis
Braya fengii
Borodinia perstellata
Arabis
nipponica
Arabis pubescens
Nasturtium
microphyllum
turgida
Murbe
ellarum
sousae
Chrysoch amel a velutina
Drab a jorulOdontarrhena
lensis
Most
acicki
llast
ca
rolinense
Odontarrhena troodi
Carda
lyrat
a
Odontarrhena cilicica Meniocu s heterotrich us
Most
acillast
rum
o rbimine
gnya
num
Alyssu m st rig osum
Carda
mine
rocki
Cardamine
rost
rata i
Alyssu m turkest anicu m
Lepidium si laifolium
CardamineEutrema
bulbosadeltoideum
Cardamine
mine simplex
hygrophila
Isatis st ylophora
Odontarrhena sch
irwanica
Bi vonaea lutea
Carda
Aethionema carneum
Alyssu
m pogonocarpu m
Mostacillastrum
ve ntanense
Goldbachia laevigata
Eu
trema
e paucifolia
Eutpseudocordifolium
rema Cardamin
wasabi
Draba rosu laris
Odontarrhena carica
Cardamine Crucihimalaya
tianqingiae
Cardamin
e cordata
Lepidium n anum
lasiocarpa multiflora
Menonvillea
norde
nskjoeldii
Cardamin
efalcata
blaisdellii
Ara
bis
cruci setosa
Carda
mine
vulgaris
Meno nvillea
cicatrico
sa
Cardamine
Heliophila latisiliqua
Crypt
osp
ora
Araperuvi
bis
sadina
Cremol
Eutrema
grandiflorum
Draba polyt
rich a obus suffrut icosus
Most
rum
dphila
ianthoides
Cardamine balnearia
Iva acillast
nia
cremno
Alyssu m moza ffaria nii
Drab
ana
Aethionema stylosum
Odontarrhena giosnana
Hemicrambe
frut iculosa
Neuontobotrys choiquens e
Drab
aagilliesii
Menonvillea marti corenae
Cardamine microphylla
Arabis watsonii
Draba acaulis
Braya thorild-wulffii
Eut rema co rdifolium
Descurainia depressa
Draba dubia
Odontarrhena huber-morat hii
Braya glabella
BorodMost
iniaaci
misso
uriensis
Drab a aspera
Noccaea nepalensis
llast
rum sa
ltaensis
Carda
mine
fulcrat
a
Aethionema spicatum
Cardamine
pattersonii
Murbecki
ella
boryi
Harmsi
odoxa
puberula
Lobularia canarie nsis
Brayafernaldii
linearis
Nerisyrenia
mexicana
Aethionema stenopterum
Most
acillastrum
h
unzikeri
Alyssu
m dasyca
rpum
Eutrema
minutissimum
Braya
Braya
qingshuiheensis
Camelina
neglecta
Cardamine
africana
Carda
mine
armoracioides
Neotorularia dentata
Cardamine jamesonii
Cardamine gunnii
Morettia canescens
Aethionema erinaceum
Physa ria mcvau ghiana
Halimol
obos
Arabis hirsuta
Drabdiffusus
a hitchcockii
Draba
thlaspiformis
Carda mine
bellidifolia
Arabidopsis
neglecta
Ara bis
paniculata
Heliophila refracta
Cardamin
e amara
Aethionema cephalanthum
Cardamine speciosa
Nast
urtium
africa
numjuressi
Cardamine
tanaka
e Ara bis
Heliophila eximia
Aethionema saxatile
Braya pilosa
Cardamin
e amarif
ormi
sa jaegeri
Aethionema munzurense
Drab
Cardamine bodinieri
Notoceras bicorne
Drab
amine
hiim
Mostacillastrum
Alyssu m simpl ex
Cardamin
e leucantha
niigatensi
s e geraniifoliava seyi
Arab
idopsi
ssmit
lyrat
aCardamin
Alyssu
thymops
Aethionema speciosum
Murbe
ckiCarda
ella
pinnatifida
Arabis
cretica lojanensis
Boe chera collinsii
Cardamin
e thomson
longipedicellata
Draba
Drabcappadocica
a harad jianii
Alyssu m ce phalotes
Cardamine
Drab
Braya
iia borealis
Nerisyrenia linearifolia
Cardamin
eiseptatum
araki
ana
Alyssu m desertorum
Draba ararat ica
Drab
a himach
alensis
Draba
bagmatiensis
odoxa
blennodioides
Alyssu m szo vitsianum
Armo
raci
a rust
PegHarmsi
aeophyton
angust
Arabidopsis croatica
Carda
mine
varia
bilis
Eut rema
sherriffii
Draba
falconeri
Drab a sunhangiana
Odontarrh ena hausskn echtii
Drab
a
arcti
caicana
Aethionema
sintenisii
Cardamine
franchetiana
Cardamine
macroca
rpa
Eutrema
fontanum
Cardamin
e torrentis
Murbecki
ella
zanonii
Cardamine granulifera
Cardamine pulchella
Dipoma
Draba
arabisans
Eut rema
yungshunensis
Eut
rema
tenue
Heliophila polygaloides
Mostacillast rum
w eberba
ueri
Cusi ckiella douglasii
Carda
mine
eremit
a iberid eum
Eutrema
integrif
olium
trema
violifolium
EutEu
rema
yunnanense
Eudema rupestris
Draba
incana
Crucihimalaya kneuckeri
Eutrema
schulzii
Nocci
dium
hastulatum
Dictyophragmus
Boechera
pygmaea
Eut
rema
lowndesi
i versico
Noccaea
lorpunensis
Eutrema
himal
aicum
Draba
arcto
gena
Cardamin
eboyacana
cheotaiyienii
Cardamine latior
Draba
Aethionema arabicum
Cardamine caroides
Noccaea
flagellifera
Neuontobotrys grayana
Drab
a
ramosi
ssima
Most acillastrum
morri
sonii
Cardamin
e
repens Bo echera rep anda
Drab a alshehbazii
Harmsi
odoxa
brevi
pes
Braya tibetica
Arab idella eremig ena
Arabis erubescens
Carda
mine
altigena
Eutrema
platypetalum
Heliophila pendula
Draba
praealta
Masmen
ia
rosu
laris
Arab
idopsis
pedemontana
Moret tia
kilianii
Cardamin
ellera
Cardamin
eacillastrum
delavayi
Bornmue
cappadocica
Cardamine
circae
oides
Cusicki ella quadrico st ata
Draba
glabella
Draba
schusteri
Aethionema fimbriatum
Most
a meghinoi
Cardamin
epanatohea
calcico
la
Hilliella hui
Draba
ides
Draba dolomitica
Lyco carpus fugax
Nocca
eaalysso
thlaspidioides
Cardamine
trif
Eu
trema
heterop
hyllum
Aethionema maraschicum
Eut
rema
wuchengyii
Draba
chamisso
nisoliolata
Arabis caucasica
Noccaea arcti
ca
Arabvenusta
isBoechera
ciliata
Noccaea
Boechera
eva dens
Boech
era rectissi
ma
williamsii
Draba barcla
yana
Cardamine Anelsonia
elegantulaeurycarpa
Cuphonotus humist ratus
Draba tomentosa
Eutrema
bouffordii
Noccaea yunnanensis
Aethionema heterocarpum
Phlebolobium macl ovianum
Drabaludlowiana
magellanica
Draba
Cardamin
e robust
Crucihimalaya tibetica
Nerisyrenia hypercorax
Carda
mine
linearil
oba a
Drab
aclematitis
inexpectata
Cardamine
Cardamin
eCardamin
digitata
Bengt-jonsellia laurentii
Cal lothlaspi
camli kense
Cochlearia
aanglica
eNocca
fargesi
Heliophila macra
eaeana
macran
Carda mine
hydroco
tyloides
Litwinowia
tenuissima
Menonvillea chilensis
Braya longii
Cochlearia tatrae
Leiocarpaea
cochleario
ides
Cardamin
brew
eri tha
Heliophila promontorii
Odontarrh ena gehamensis
Draba ishkomania Cardamine diphylla
Metashangrilaia forrestii
Abd ra
aprica
Noccaea andersoniiArabidopsis arenosa
Carda mine engleria
na
Be ngt-jo nse llia tsarat ananae
Ara
bis umezewana
Arabis
olympi ca
Bornmue
glabresce
Carda
mine
yunnanensis
Cremol obus rhomboideus
Drabllera
a palanderia
nans
Aethionema monospermum
Aethionema
capitatum
Ammosperma cinerea
Neotorularia
brevipes
Arabidopsis petraea
Cardamineauricul
magni fica
Drab
a bracke
gei
Arabis
pycnocarpa
Goldbachia pendula
Physaria purpurea
Nocca
ea
birol
mutlui
Cardamine
ata
Arab
isnrid
nova
Arab
is
montbret
iana
Drab
akomarovi
murra
yi i
Ara
bidopsis
icola
Cardamin
e aren
Berte roa orbiculata
Draba
Cardamine
pensyl
vanica
Cuphonotus andraeanus
Noccaea
aptera
Arab
Drabpennellii
a lact
ea is kawasaki ana
Noccaea rotundifolia
Alliaria
petiolata
Aethionema rhodopaeum
glechomif
Cardamin
eolia
lihengiana
Lepidium perfoliatum
Cardamine
scutata
Draba
oreibata
eathera
jaubertii
Pa rlaNocca
toria
cakiloidea
And rzeiowski Cardamine
a cardamin
ifolia
Cardamine
micran
Drab a howellii
Arabidopsis suecica
Carda
mine
flexu
osa
Heldreichia bupleurifolia.rotundifolia
Cardamine griffithii
Draba
dedeana
Noccaea annua
Nevada
holmgren
ii
Nocca ea
grif fithiana
Chrysoch amela noeana
Heliophila trifurca
Ara bis drabiformi s Nocca
Drab
a mulliganii
Eu nomia iberid ea
Cardamine
changbaiana
parvif
lora
Christolea crassifolia
Cardamine
umbellata
Drabea
a subnivalis
Ivania
juncalensis
Draba steyermarkii
Cardamin
euaria
alpina
ArabBo
isrodinia
aucheri
Crambella
Draba
depressa
Cochlearia
aest
Draba soratensis
Drab a Carda
siliquosa
Arabidopsis
halleri teretifolia
canadensis
Draba
argentifolia
Draba
porsil dii
Drab a sa kuraii
mine nipponica
Cardamine papuana
Menonvillea comberi
Aethionema eumomioides
Cardamin
ea stenoloba
rodinia
laevi gata
DrabBo
lapaziana
Helioebract
philaeata
laciniata
BoCarda
rodinia
burkii
Dilophia
Ammosperma variabile
Cuprella homalocarpa
mine
plumie
riDraba
Cardamine jonselliana
Aethionema demirizii
Alyssu m margi natum
Eu
trema
halophilum
Eutrema
salsugineum
Carda
mine
parvifoblongata
lora
Noccaea ochroleuca
Noccaea occitanica
Arabis alanyensis Cardamine keysser i
Chrysoch amela elliptica
Pa
chycladon stellatum
Cochlearia
pyren
aica
Pet rorave nia eseptata
Menonvillea rigida
rema
nepalense
Noccaea
vesicaria
Heliophila namaquensis
Carda mine occidentalisEutDrab
Heliophila dregeana
Aethionema
papillosum
a monoensis
Neotorularia
contortuplicata
Draba
kluanei
Lepidium serratum
Cardamine
obliqua
Nasturtium
officinale
Hemilophia franchetii
Heliophila rigidiuscula
Ara bismagaliesbergensis
patens
Bornmue
llera angustifolia
rema japonicu
m
Dimorphocarpa candicans
Heliophila
Iberis umbellata
Catolobus
pendulus
Heliophila tulbaghensis
ExhaEut
limolobos
arabioides
Borod
inia
serotina
Aethionema glaucinum
Moret
tia parvifloraDrab
a norveg
ica
Ara bis
bellidifolia
Lepidium b arnebyanum
Hormathophylla spinosa
Noccaea cochlearioidea
Ionopsidium g lastifolium
Lepidium
b ipinnatum
Eutrema edwardsii
Parodiodoxa chionophila
Cochlearia borzae ana
Noccaea
magellanica
nubigena
Nocca
ea microst
ylaDrab a cinerea
dentata
Ara
bis auricu lata Bo rodinia
Heliop hila obibensi s Eudema
Heliophila brassicifolia
Oreophyton falcatum
Arab
is allionii
Pach yphrag ma macrop
hyllum
Heliophila gariepina
Menonvillea virens
Draba violacea
Mostacillast
rum
f erreyrae
Draba
nivalis
Drab
a funiculosa
Draba
lonchoca
rpa
Cochlearia
danica
Cochlearia
officinalis
Notothlaspi australe
Heliophila clarkii
Cardamin
e rupicola
Ionopsidium aragonense
Maresia nana
Drab a mie heorum
Farsetia burtonae
Drab
a ucuncha
Aethionema membranaceum
Aethionema lycium
Drab
a crypt
antha
Cochlearia polonica
Drab
a hookeri
Crambe kotschyana
Helio phila suborbi cularis
Hormathophylla baetica
Cardamine flaccida
Heliophila tricuspidata
californica
Draba
subcapitata
Dilophia salsa
Bornmue llera kiyakii
ocarpa
DrabDimorph
a burkarti
ana pinnatifida
Drab ast rum a lpestre
Heliophila
seselifolia
Arcyosperma primulifolium
Drab a si kkimensis
Ca melina
stiefelhagenii
Lepidostemon gouldii
Hormathophylla
reve rcho nii
Aphragmus serpens
Cardamin e chenopodiifolia
Graellsia chitral
ensis
Asp eruginoides
axillaris
Ihsanalshehbazia
granatensis
Carda mine rot undifolia
Heldreichia bupleurifoli
Heldreichia ba.bourgaei
upleurif olia
Heliophila glaucaHeliophila ramosissima
Alyssu m paphlagonicum
Capsella
granstdflora
Neurotropis orbiculata
Drab a winterbottomii
Draba cana
Grae
llsia
ylosa
longicaulis
Ionopsidium acaule
DimorphHormathophylla
ocarpa membran
aceae
Lepidium
brach
yotum
Aethionema saxatile.creticum
Pachymitus cardaminoides
Cardamin
e
flagellifera
Anast
atica
hieroch
untica
Exha
limolobos
palmeri
Exh
alimolobos
polyspermus
Menonvillea frigida
Graellsia
Cardamin e bonariensis Neotorul aria torul osa Hollermayera valdiviana
Exha
limolobos
parryi
Cardamin
eisfahan
jejuna
Graellsia
olia
Mostacillastrum h aitiense
Mostaci
llast
rumintegrif
p ect
inifolium
Lepidium jujuyanum Hilliella
Mancoa
ve
nturii
lich
uanensis
Eutrema hookeri
Hemilophia pulchella
Draba ussu rie nsis
Braya rosea
Aethionema diastrophis
Chilocardamum p atagonicum
Lepidium
fHeliophila
remon
tiijaegeri
Halimolobos
Cardamin
epapilliferum
mexi
cana
Heliophila suavissima
Grae
llsia
hissarica
Lepidium
Lepidium spinosum
Graellsia
Graellsia
saxifrag
longistyla
ifoliaastyla
Grae llsia
graellsi
ifolia
Heliophila
minor
Arabis arabiformis
Hornungia Draba
alpina subamplexi caulis
HilliellaHilliella
sinuata
sinuata
sinuata
Dimorphocarpa wislizeni
Drab a subalpina Cardamin
Noccaea fendleri
Chilocardamum
oqianwuensis
nurid
ifolium
Heliophila
volki
i
tryssaocculta
Cardamine innovans
Cardaemine
Draba confertifolia
Heliophila
pseudoexi
mia
Cardamine astoniae
Lepidium
CardaLepidostemon
mine chilensis
Hilliella
rup
Chilocardamum
caparadoxa
st
ellanosii
Clypeola lappacea
Boicola
tsch
antzevia
ka ratavica
rosusch
larislech teri
Braya
humilis
Cardamine
margi
nata
Cardamine
oligosperma
Hi
lliella
Crambe arborea
Baimashania pulvinata
Capsella
thraci
Cardamine franklinensis
Carda
mine
krue
sseca
lii
Heliophila
bise
Draba stylosa
Noccaea nevadensis
Lepidium
friata
erga
nense
Aethionema subulatum
Heliophila
xylopoda
Notothlaspi viretum
Cardamine
impatiens
Manco
a
Lepidium
lacerum
Noccaea brevistyla
Graellsia davisiana
Capsella
Capsella
bursap
asthispida
ntalis
oris
Heliophila brachycarpa
Hi
lliella
yi xianensi
s orie
Mancoa
foliosa
libyca
Neurotropis platycarpa
Cakile arabica
Hormathophylla purpurea
Draba lance olata
Hilliella
rivuLobularia
lorum
Aethionema saxatile.ovalifolium
Drab a juvenilis
Eunomia oppositifolia
alepense
Lepidium
ppelianum
Lepidium
astwoodiae
Pe nnellia lech leri
Hormathophylla spinosa
Euhunanensis
trema each
botsch
antzevii
Alyssum tetrastemon
Cremol
obusHilliella
bolivianus
Heliophila
collina
Drab lasi
a parvif
sekiyana
Draba
lora
Draba
ophylla
Noccaea brachypetala
Cardamine uniflora
Draba
turczan
inowii
Drab a fladnizensis
Drab aDraba
lichiangensis
Murica ria postrat a
ladyginii
Heliophila deserticola
Eut rema altaicum
Draba glomerat a
Cardamine bisetosa
laegaardii
Coch learia sessi
lifolia d avisii
Draba splendens
Menonvillea
zuloagaensi Draba
s
Lepidium
Cardaminmeye
e tenuifolia
Lepidium
nii
Heliophila remotiflora
Aphragmus minutus
Carda mine holmgren
ii beckii
Neuontobotrys l anata
Lepidium
Lepidium
heterophyllum
Aphragmus oxycarpus
Abdra brach yca rpa
Petrocallis pyrenaica
Ara bidopsis thaliana
Lepidium
huberi
Heliophila cinerea
Aethionema huber-morathii
CremolCremol
obus su
bscachilensis
ndens
Lepidium
thurberi
Cardamin e hirsut a
obus
Cardamine chelidonia
Draba
breweri
Drab a handelii
Pach ycl adon cheesemanii
Cardamine trifolia
Menkea
crassa
Draba ca jamarcen sis
Menonvillea
patagonica
Draba
macleanii
Sphaeroca rda mum fruticul osum
Eru cast rum l eucanthum
Cochlearia
groe
nlandica
Drab a ellipsoidea
mine
debilis
Draba
yukonensis
ladakianus
Menonvillea famatinensis
DrabAphragmus
aCarda
kitadakensi
s rot undum
Heliophila
pectinata
Lepidium
Menonvillea minima
Sp haeroca rdamum co mpressu m
Cochlearia
trid actylites
Drab
pycnophylla
Draba hemsleyan a
Drab
a atucumanensis
Aphragmus hobsonii
Cardamine
microt
hrix s alysso ides
Draba picke ringii
Lepidium
Hilliella shuangpaiensis
Murbeckie lla huetii
Carda mineMancoa
moirensi
Draba ecuadoriana
chlearia
mica
cea
Pen Co
nellia
parvifbract
lora eata
Eut rema
Drabananum
longiciliata
Drab a loayza na
Heldreichia
Cardamine subcarnosa
Draba sco
pulorum atalayi
Heliophila pusilla
Draba hallii
Sphae roca rdamum ramosum
Lepidium i ntegrif olium
Eudema incurva
Hilliella fumario ides
Draba se rice a
Sphae roca rdamum macr opetalum
Noccaea stenoptera
Callothlaspi cariense
Lithodraba mendocinensis
Lepidium flexuosum
Lepidium
olerace
um
Sphaeroca rdamum divar icatum
Manco
a laeviis
s w erff ii
Cardamin e chlorin a
Drabella
mural
Lepidium
Draba doerfleri
Braya
alpina karamanicum
Eruca strum rif anum
Aethionema
Ara bis tanakana
Heliophila linearis
Baimashania wangii
Aphragmus obscurus
Pa ysonia
stonensis
Payso
nia perfo
rata
Ara bis se rpyllifolia
Arabis caerulea
Heliophila
tabularis
Ara bis surcul osa Cardamine alticola
Megadenia
pygmaea
Cardamine pancicii
Lepidium e ckl onii
Hornu
ngia procu
mbens
Braya parvia
Aimara rollinsii
Carda
mineLepidium
coron
ata
Engleroch
aris
dentata
Aphragmus bouffordii
Heliophila crit hmif olia
Lepidium
mossi
Lepidium
myri pinnatum
ocarpu
Hormathophyl
la lapeyrou
siana m
Lepidium n aufragorum
Dactylocardamum polyspermum
Heliophila leptophylla
Ara bis scabra
Eucl idium syria cum
Lepidium foliosum
Cardamin e alalata
Arabis alpina
Drab a quearaensis
Heliophila bulbostyla
Lepidium sa tivum Lepidium t enuicaule
Ionopsidiu m megalospermum
Berte roa incana
Heliophila crassistyla
Heliophila linoides
Drab a orie ntalis
Cardamin e glacialis
Draba spruce ana
Cardamine volckmannii
Athysanus unilateral is
Drab a disco idea
Hormathophyl
cadevalliana
Cardamine guatemalensis
Christ olea
niyaLepidium
ensis laostleri
Eng leroch aris anca shensis
Noccaea sintenisii
Drab a altaica
Dryopetalon byei
Heliophila arenosa
Aethionema retsina
Exh alimol obos pazense
Heliophila lactea
Noccaea Noccaea
valerianoides
Cardamine hupingshanensis
Lepidium
turczan inowii
Heliophila carnosa
caerulescens
Didymophysa fedtsch
enkoana
Ara bis marga rit ae
Pa chycladon
exile
Aphragmus ohbanus
Eng leroch aris blanca-leoniae
Kerne ra boissieri
Drab a punoensis
Heliophila elata
Ladakiella klimesii
Exha limolobos burkarti i
Descu rainia canoensis
Dryopetalon palmeri
Draba inquisiviana
Arabis parvula
Lepidium aegrum
Odontarrhena
st ipitata
Drab a stylaris
Lepidium
o abtusatum
Lepidium
oblitum
Lepidium
cu
zco
ensis
Atela nthera perpu silla
Lepidium
ustrin
um
pilosulum
Capsella Microl
rubellaepidium
Iren epharsus magicus
Kernera saxatilis
Noccaea tatianae
Lepidium b anksii
Heliophila meye ri
Crambe filiformis
Eud ema peruvi ana
Coronopus navasii
Aphragmus eschscholtzianum
Heliophila minima
Brayo psis alpaminae
Ast a sch affneri
Menonvillea litoral
is
Aphragmus pygmaeus
Heliophila
pubesce
Cardamin e glauca
Lepidiumnslimenophylax
Lepidium cren atum
Lepidium ca espitosu m
Lepidium p etrophilum
Ch ilocardamum
Lepidium h owei-in sulae
Lepidiuml ongistylum
st ylatum
Lepidium
Lepidium
aucheri
Exh alimolobos berla
ndieri obtusum
Heliophila subulata
Lepidium pumil um
Crambe kralikii
Noccaea papillosa
Lepidium
hirtu mpinnatifidum
Lepidium
Draba obova ta
Lepidium rig idum
Noccaea sylvia
Calepina irregularis
Lepidium ve si cariu m
Lepidium latifolium
Lepidium villarsii
Carda mine longii
Peltariopsis planisiliqua
Dryopetalon membranifolium
Heliophila descurva
Cardamin
e lacu stris
Lobularia marit ima
Kotsch
yellamaka
stenoca
Lepidium
l yratrpa
um
Lepidium
teanum
Dryopetalon breedlovei
Drab a mongolica
Crambe
grandiflora
Lepidium
ca rdamines
Lepidium
alashanicum
Dryopetalon paysonii
Mostacillastrum
gracile
Dryopetalon crenatum
Lepidium
ca rti lagineum
Diptychocarpus strictus
Aubrieta deltoidea
0.0
Arabis mcdonaldiana
Cardamine acris
Cardamine
macrophylla
Cardamine angustata
BrachypusArabis
suffruticosus.tabriziana
aculeolata
Cardamine nuttallii
Boechera
johnstonii
Boechera
lincolnensis
Boechera
subpinnatifida
Parryodes axilliflora
Cardamine violacea
Boechera parishii
Heliophila maraisiana
koehleri
Boechera
fecunda
Boechera
sparsiflora
Boechera
xylopoda
Cardamine loxostemonoides
Cardamine quinquefolia
Alyssu m neglectum
Drab a remot iflora
Bra ssica frut icu losa
OtocarpusDraba
virgatus
Draba cheiranthoides
Draba
bhutanica
cholaensis
Boechera rollei
Cardamine luxurians
Cakile edentula
Hesperidanthus jaegeri
Erysimum baeticum
Heliophila cuneata
Marcus-kochia ramosissima
Aubrieta glabrescens
Aubrieta sicula
Diplotaxis acris
Eru cast rum n asturtiifolium
Al yssu m n ezaketiae
Alyssu m doerfl eri
Brassi ca nigra
Drab a cret ica
Barba rea trich opoda
Phlegmat ospermum co chlearin um
Arabis collina
Marcus-kochia parviflora
Malcolmia orsiniana
Hesperidanthus linearifolius
Iodanthus pinnatifidus
Aubrieta intermedia
Aubrieta italica
Aubrieta scardica
thessala
Aubrieta
scyria
Aubrieta
alshehbazii
Aubrieta
pirinica
Aubrieta
Aubrieta
macrostyla
olympica
Aubrieta
Aubrieta
canescens
croatica
cilicica
Aubrieta anamasica
Aubrieta gracilis
Aethionema armenum
Aethionema coridifolium
Diplotaxi s siettiana
Physa ria geyeri
Physa ria alpestris
Physa ria lepidota
Alyssu m b ornmue lleri
Barbarea grayi
Camel ina alyssu m
Cardamin e grae ca
Erucaria hispanica
Erysimum pallasii
Diplotaxis griffithii
Arabis oregana
Cardamine heptaphylla
Erucaria ollivieri
Aubrieta bulgarica
Aubrieta pinardii
Aubrieta columnae
Aethionema grandiflorum
Megacarpa ea polyandra
Barbarea taiwaniana
Diplotaxi s berth autii
Barba rea vernaBarba rea hongii
Megaca rpaea bifida
Heliophila scoparia Barba rea strict a
Oct oceras Nasturtiopsis
lehmannianum
integrif olia
Alyssu m rho danense
Alyssu m harpu ticu m
Biscutella variegata
Alyssu m orop hilum
Hugueninia tanacetifolia
Bra ssica elongata
Odontarrhena masmen aea
Isa tis huber-morat hii
Isatis const rict a
Alyssu m macroca lyxDrab a daviesiaePhysa ria filiformis
Eru castrum e latum
Alyssu m cu neifolium
Isatis busch iana
Alyssu m propinquum
Camel ina laxa
Isatis quadria lata
Alyssu
Neslia panicu lata
Alyssu m hirsut
umm st rib rnyi
MeniocuBiscu
s aureus
coronopifolia
Altella
yssu m
ka ynakiae
Isatis st ocksi i
Al yssu m co rningii
Draba carnosu la
Isatis davisiana
Alyssu m su lphureu m
Erysi mum ch eiranthoides
Odontarrhena condensata
Isa tis lusitanica
Draba yungayensis
Drab
a helleriana
Draba crassa
Alyssu m f oliosum
Alyssu m caespitosum
Draba
maguirei
tella atlantica
Biscu tellaBiscu
frutescens
Draba arau quensi s
Isa tis harsukh ii
Drab a pterosp erma
Draba amplexicaulis
Drab a spectabilis
Nast urtiopsis coron opifolia
Biscu tella marin ae
Draba jucu
Odontarrh ena trap eziformis
Drabnda
a polyphylla
Ba rbarea bract eosa
Chorisp ora tashkorga
nica
Petrorave nia frie sii
Biscutella
Biscumaestratensis
tella
Bisculaevigata
tella
laxa ena roberti ana
Drab a surcul osa
Drab a weberi
Odontarrh
Draba pachyt hyrsa
Isatis co stata
Biscu
tella rot gesii
Draba venezuelana
Engleroch aris cuzco ensis
Meniocus meniocoides
Isatis emargi nata
Draba
abajoensis
DrabaDrab
chionophila
Drab
aalpina
heilii
Draba
Drab
pilosa
Draba
se
sharsmi
rpentina
thii
Drab
apetrophila
asprella
Drab a lemmonii
Al yssu m ca cumin um
aaasco
tteriis
Draba
incerta
Draba
Camelina hispidaDrab a pect inipila
Draba
virid
Drab
atrinervis
burkei
Drab
ventosa
Drab
siammonsi
i
Drab
aaaffghanica
Drab
aDrab
aubrie
toides
Descurai nia kochii
Alyssu m aizoides
Drab a streptobrach ia
Draba
argyrea
Isatis mul ticaulis
obtusifolia
Alyssu m
a rmenum
Biscu tella
tellaOdontarrhena
glacialis
chondrogyna
Drab
a standleyi
Draba
beltranii
Biscu
calduchii
Alyssu m Odontarrhena
pirin icum
Drab a cycl omorph a
Drab
sobolifera
Drab
aa
aurea
Drab
aaexunguiculata
Biscu tella marit ima
Drab a senilis Lepidost emon glarico la
Isatis min ima
Drab
arid a
Isa tis glauca
Drab a ramul osa
Drab a pedicellata
Drab
aNeuontobotrys
densifolia
Draba
globosa
Isatis brevi pes
Isatis gymno carpa
Draba
gramin
ea ca manaensis
Petrorave nia werdermannii
matangensis
Eruca st rum b revi rost re
DrabDraba
a aretioides
a graya
Descu rainia pinnata
DrabDrab
a brach
yst ylna
is
Arab idella trise ct a
Odontarrhena akamasi
discolorca
Alyssu m co ntemptum
Drab
a stenoloba
Odontarrhena
Drabpedunculosus
a calci cola
Drab a canoensis
Lepidost emon
Draba
albertina
Odontarrhena strid ii
Isatis glast ifolia
Alshehbazia hauthalii
Drab
a mogollonica
Camelina microca rpa
Alyssu m f astigiatum
Draba novolympica
Odontarrhena erio phylla
Draba alajica
Alyssu m l oiseleurii Draba
Draba
pusilla
paucifruct
a
Odontarrhena
pateri
Alyssu m diffusum.ca labricu m
Biscu tella lyrat a
Draba corrugata
Odontarrhena florib unda
Draba payso nii
Drab
a tibetica
Biscu tella
Drab a streptoca rpa
Biscu tella pseudolyrat
a microca rpa
Descu rainia sophia
Draba
si birica
Draba
oreodoxa
Isatis ornitorhyn chus
Odontarrhena
tortuva
osa
.tortu osa
Borea
aptera
Biscu tella semperviren s
Odontarrhena const ellata
Drab a ko ngboiana
Odontarrh ena alpestris
Draba extensa
Biscu tella fontqueri
Odontarrhena pteroca rpa
Odontarrhena mural
is
Odontarrhena
sza rabiaca
Alyssu m diffusum.garga nicum
Odontarrhena tortu osa.heterophylla
Isa tis demirizi ana
Alyssu m granatense
Draba zionensis
Odontarrhena
Odontarrhena berto
arge
ntea
lonii
arbuscu la
DrabaDraba
malpighiacea
Odontarrhena
sa marif era
Odontarrhena syria ca
Draba sp haeroca
rpadraboides
Draba yunnanensis
Draba
Drab a ast erophora
Alyssu m diffusum.diffusum
Descu rainia antarcti ca
Draba grandis Ara bidella nast
Alyssu m rosse tii
urtium
Drab a humil lima
Biscu
tella turolensi
alcaerodiifolia
rriaes
Draba santaquinensis
Odontarrhena corsica
Draba
osa elata
Descurainia
Biscu
tella
Drab acorymb
cachemirica
Alyssu m sp runeri
Alyssu m xa nthocarpu m
Draba
ogilviensi
si
Drab
aDraba
linearif
olia
Odontarrhena
peltariovirgata
idea.virgatiformis
a cruci
Odontarrhena
subspinosa
Bra
ya Drab
sch
arnh
orstiata
Biscu tella ebusitana
setosa
Drab
aDraba
Odontarrhena
Alyssu m maza ndaranicum
Drab
astenocarpa
cusicki
i
Drab aDrab
longisquamosa
Al yssu m l enense
a trich
ocarpa
Descurainia nuttallii
Alyssu m nevadense
Draba involucrat a
Drab a oligosperma
idella procu mbens
Biscu tella
Biscuneustria
tella molcalis
Alyssu mArab
atlanticum
Draba macb eathiana
Camelina rumel ica
Odontarrh enachalcidica
deci piens
a nuda
Drab
a Drab
melanopus
Drab
maco
unii
Biscu tella atrop urpurea
Odontarrhena
peltario idea.peltarioidea
Odontarrhena
Drab
aensis
erio
poda
Descu rai nia paradisa
Glastaria glastifolia
Drab
aacuzco
Drab a olgae
Biscu tella baetica
Draba cemil eae
Drab
a nemorosa
Odontarrhena anatolica
Drab
a rectifruct
Odontarrhena cyp rica Odontarrhena lesbiaca
Alyssu m min utum
Drab a huetii
Conrin gia persica
Alyssu m g adorense
Drab
a barth
olomewii
Drab a pauciflora
Cuprella antiatlantica
Draba
za ngbeiensis
Odontarrhena
oxicarpa
Alyssu m a ertvi nense
Cremol obus peruvi anus
Drab a oxyca rpa
Biscu tella intermedia
Drab a microp etalaMyagrum p erfoliatum
Drab a hispida Drab a rig ida
Meniocus linifoius
Al yssu m macrop odum
Drab a st enopetala
Odontarrh enaserpyl
pinifolia
Odontarrhena
lifolia
Menkea
vi llosula
Odontarrhena
smol ika na Draba cantabria e
Descu rainia virle tii
AlAlyssu
yssu mmsmyrn
aeum
f ulvesce
ns
Descu
rai nia sophioides
Odontarrhena
cassi aii
Odontarrhena
dubertret
Draba oreades
Odontarrh ena fallacina
Hemicrambe socotrana
Menkea lutea
Draba thylocarpa
Odontarrhena mural e
Arab idella filifolia
Odontarrhena fragillima
Alyssu m p lusca nesce ns
Biscu tella ambigua
Alyssu m erosu
lum
Alyssu m aust rodalmat icum
Camelina sativa
Clypeola cycl odontea
Odontarrh ena filiformi s
Odontarrh
ena orbelica
Most acillastrum a ndinum
Odontarrhena albiflora
Al yssu m gmelinii
Eun omia caespitosa
Drab a graci llima
Alyssu m st rict um Odontarrhena borzae ana
Diplotaxis
ides
Drabaeruco
korshi
nskyi
Alyssu m t ortu osum
Ochtodium aegyptiacum
Odontarrhena davisiana
Odontarrh ena nebrodensis
Draba sierra e
Lepidostemon everest ianus
Descu rainia
Alyssu m aurantiacum
Odontarrhena morave nsis
Bi scu myri
tella ophylla
prealpina
Nast urtium florid anum
Neuontobotrys
ulzii
Odontarrhena
sibirica
Odontarrh ena
rigida
Drabsch
a saxosa
Descu rainia adenophora Descu rainia torulosa
Phlegmatospermum rich ardsi i
Drab a sphaeroides
Alyssu m scu tigerum
Descu rainia Descu
longepedicellata
Descurainia
incisa
rai nia impatiens
Odontarrhena callichroa
Hormathophylla cochleata
Neuontobotrys i ntrica tissi ma
Descu rainia st reptocarpa
Odontarrh ena dudleyi Biscu tella brevi caulis
Lepidium patrin oides
Alyssu m min us
Alyssu m flahaultianum
Draba elegans
Descu rainia pimpinellifolia
Descu rainia st rict a
Drab a subumbellata
Camel ina anomala
Descu
rainia
incana
Odontarrhena cren ulata
Descu
rainia
pumil folia
a
Descu
rainia
breviobtusa
siliqua
Lepidium tiehmii Olimarabidopsis
Alyssu m lanceolatum
Draba
Drabacrassi
lutesce ns
Descu rainia ca lifornica
Draba hispanica
Olimarab idopsis cabulica
Descu
kenheilii
Descu
rairainia
nia nelsonii
Lepidium flavum
Mostacillastrum oleraceum
Cardamine bulbifera
aridanae
Parolinia Parolinia
schizogynoides
Orychophragmus diffusus
Malcolmia africana
Cardamine granulosa
Cardamine nepalensis
Fortuynia bungei
Dontostemon
elegans
Megacarpaea
megalocarpa
Chorispora sabulosa
Parrya golostebelnaya
Crambe wildpretii
Eruca setulosa
Orychophragmus ziguiensis
Chorispora greigii
Erucaria crassifolia
Boechera yorkii
Parrya pazijae
Neuontobotrys
l inearif olia
Neuontobotrys
e lloanensis
Drab a nylamensis
Diplotaxis
ollivieri
Diplotaxis
ilorcit
ana
Drab a cryop hila
ina
Barbarea
Barba rea
anfract
auricu
uosa
lata Brassi ca oxyrrh
Barba rea rup icola
Draba
cuatreca
Erysi
mum visasiana
rgatum
Malcolmia chia
Chorispora tenella Eremobium aegyptiacum
Marcus-kochia patula
Hesperis cilicica
Blennodia canescens
Heliophila pinnata
Diplotaxis glauca
Eru cast rum g allicum
Arabis modesta
Dontostemon hispidus
Erucaria erucarioides
Parrya fruticulosa
Parrya pulvinata
Parrya schugnana
m
Brassi ca junce a
Alyssu m argyrop hyllum
Physa ria acu tifolia
Menonvillea purpurea
Draba lindenii
Neuontobotrys b erningeri
Menonvillea linearis
ka melinii
g raecum
ErysimumErysimum
se Erysimum
rpentinicum
Erysimum
nconspicuum
Erysi
mummse iipkae
Erysi mum mon
golicu
Erysi mum b enthamii
Erysi
mum pcaonticu
chemiricu
Erysimum
m m
Erysi mum macrost
igma
Menonvillea orbiculata
Erysi
mum
marscha
llianum
Erysimum
krynke
nse
mum myri
Erysi mum Erysi
p enyalaren
se ophyl lum
edebourii
ErysiErysimum
mum szol vitsianum
Erysimum
w owski
elceviii
Erysi
mum red
Erysi
mum
g ladiiferum
Erysimum
virossi
tellinum
Erysi
mum
cum
Erysi
mum
sp etae
Ca rdamine enneaphyllos
AnchErysi
onium
elichrysif
olium.e
lichrysif
olium
mum
cret
icum
Erysi
mum
ca
llicarpu
Erysi
mum
crassim
ca ulemum
Erysi
mum
f rohneri
Erysi
st rict um
Erysimum
ko m
elzii
Erysimum
ca
espitosu
Erysimum n evadense
Erysimum
va
ssi
lczenkoi
Diplotaxis kohlaanensis
Erysi
mum
e lbruse nse
Erysimum
b laabadagense
Erysimum
azist
anicum
Erysi
mum
bsco
nditum
Erysimum
p ersep
olitanum
Erysi
mum aasianum
Erysi mum
h ajastanicum
Physa ria crassi stigma
Erysi
mum
anceps
Menonvillea pinnatifida
Erysisa
mum
babataghi
Erysimum
langense
filifolia
Erysimum rep
andum
b dicum
adghisi
Erysi
mumErysimum
sa markan
Erysimum
o lympi
cum Menonvillea
Erysi
mum
co
Erysi
mum
ch azarju
Erysimum
ca arcta
riurtimtum
Erysi mum
a ndrzej
owski
anum
Erysi
mum
l leptophyllum
Erysi
mum
onicum
Erysimum
uyca
cran
icum
Erysi
mum
gelidum
Erysimum
si mum
ntenisianum
Menonvillea const
itutionis
Erysi
so
rgerae
Erysi
mum
rau
linii
Erysimum
ungaricu
m
Erysi
mum
Erysimum
sth enophyllum
t enellum
Erysimum
i nense
Erysi mum
cu spidatum
Erysi
mum styl
d eflexum
Erysi
mum
g ypsaceum
Erysi
mum
crassi
um
Brassi ca cret ica
Fibigia clypeata
Microst
igma
brach
yca rpum
Payso nia lasiocarpa
Anchonium
elichrysif
olium.vi llosum
Erysimum
rba
baevii
Erysi
mum
llunarioides
eptostylum
Acust
onke
Pa ysonia gran diflora
Erysimum
o
leifolium
Erysi
mum
lntale
eptocarpum
m
Erysi
mum
hbulgaricu
orizo
Erysimum a znavourii
Erysi
mum
uphrat
icum
Erysi
mum
suemicrost
bstrig
osum
Erysi
ylum
Erysi
mum
ca
ucasicum
Erysi mum
umum
ncinatifolium
Erysi
mum
d mum
egenianum
Erysi
mum
e ginense
Erysi
w ilcze kianum
Erysi
mum
a rmeniacum
Erysi
mum
roba ustum
Erysimum
ureum
Hemilophia sessi folia
Erysi
mum
vinense
Erysi
mum
ranicum
Erysi Erysi
mum
macrosp
mum
a dcumbens
Physa ria pygmaea
Chorisp ora sibirica
Erysi
peiermum
ulchellum
Erysimum
schmum
lagintweitianum
Erysi
mum
e rosu m
Erysi
mum
crep
Erysi
mum
i dae
Erysimum
sca
brum
Erysimum
bidifolium
oissieri
Erysimum
iksa
raqense
Erysi
mum
aamum
rtw
Erysimum
nchinellum
abievii
Erysimum
Erysi
mum
e
dinense
iffusum
Erysi
boreale
Erysimum
ricu m
Erysi mum grif fithii
Diplotaxis pitardiana
Erysimum a crot onum
Barba rea orth oceras
Neuontobotrys t arap acana
Fibigia
Fibigia
macroca
erio
carpa
rpa
Erysimum
rdicum
Erysi
mum
gku
oniocaulon
Erysimum
i sch
nostylum
Erysimum
ca spicumMenonvillea macroca rpa
Erysimum
l eucanthemum
Erysimum mut abile
Draba humbertii
crassi
pes
ErysiErysi
mummum
n asturti
oides
Barba
rea potaninii
lutea
Erysimum a uchGalitzkya
eria num
Eruca
strum
rabicum
Erysimum
koa
st
kae
Erysimum
axiflorum
h lakki
aricu
m
ErysimumErysimum
nErysi
emrutdaghense
mum
g haznicum
Erysimum
f rig idum
Erysimum a denocarpum
Eruca strum st rig osum
Menonvillea flexuosa Diplotaxis ibicensi s
mum
brevi
stylum
ErysiErysi
mum
hirschf
Erysi
mum
sueldioides
bulatum
Erysimum
h ieraci
ifolium
Erysi mum a fghanicum
Bra ssica glabresce ns
Hesperid anthus su
ffrutesce
Erysi
mum gnsrif fithianum
Eruca strum g riq uense
Ba rbarea australis
Erysi mum h uber-morat hii
Barba rea integrif olia
Draba farset ioides
Erysimum maci lentum
Erysimum
homsonii
Diplotaxis simplex
Erysi mum
st ocksit anum
Barba reaDrab
minor
a bellardii
Erysi mum si symbrio ides
Ena rth roca rpus lyrat us
Bra ssica gravi nae
Brassi ca barrelieri
Barba rea sicula
Barba
Barbarea
reaplantaginea
platyca rpa
Crambe gordjaginii
Parolinia ornata
m
Hirschfeldia incana
Bra ssi ca balearica
Alyssu m lepidotum
Barba rea intermedia
Bi scu tella auricu lata
Cardamin e kitaibelii
Erysi mum amuren se
Erysimum
e yanum
tnense
Erysi
rusci
nonense
Physa
ria mendocina
Erysi mum
mum
ko tsch
Erysi mum odorat um
Erysimum e truscu m
Erysimum
f itzi iEru castrum va riu m
Brassi
ca repanda
Erysi mum
mum
ca nesce
ns
Erysimum p achyca
rpum
Erysi
mum
a laicum
Erysi
meye
ria num
Erysimum q uadran gulum
Hesperis turkmendaghensis
Moricandia rytidocarpoides
Erucaria
cakiloidea
Parrya
glabra
Cardamine calliphaea
Microstigma
deflexum
Microstigma
sajanense
Hesperis theophrasti
Erysimum lagascae
Marcus-kochia littorea
Heliophila juncea
Aethionema thesiifolium
Brassica loncholoma
Hemilophia rockii
Leiospora exscapa
Leiospora pamirica
Hesperis anatolica
Parrya pinnatifida
Hesperis matronalis
Hesperis luristanica
Hesperis aspera
NMDS2
Erysimum limprichtii
Malcolmia flexuosa
Diceratella canescens
Matthiola parviflora
Hesperis ozcelikii
Hesperis bicuspidata
Parrya nudicaulis
Erysi mum t eret ifolium
Erysi mum w ardii
Erysimum
g omezca
Fezia pteroca
rpa mpoi
Erysimum i nsu lare
Diplotaxis va ria
Erysimum
a itchisonii
Erysimum
a ltaicum
Brassi ca spinesce
ns ca cret ica.laconica
Brassi
Neuontobotrys rob ust a
Physa ria okanensis
Leavenworthia uniflora
Douepea arabica
Petiniotia purpurascens
Hesperis pseudoarmena
Hesperis persica
Di plotaxis su ndingii
Erysi mum d amirli ense
Cerat ocnemum rap ist roides
Cordyl ocarpu
tus
Brassi scamurica
cret ica.aegea
Erysi mum si liculosum
Physaria lateralis
Matthiola torulosa
Matthiola tricuspidata
Matthiola daghestanica
Diceratella flocossa
Matthiola bolleana
Parrya lancifolia
Erysimum g eisl eri
Brassi ca carin ata
Bra ssi ca aucheri
Erysimum senoneri
Hesperis kotschyi
Matthiola montana
Matthiola stoddartii
Matthiola
perpusilla
Moricandia
suffruticosa
Erysimum a sperum
Erysimum f lavum
Lutzia cret ica
Erysi mum rho dium
Erysimum mel icentae
Erysi mum rha eticum
Erysimum g orbeanum
Diplotaxi s graci lis
Diplotaxis vogelii
Cardamine pentaphyllos
Parrya rydbergii
Matthiola pumilio
Matthiola sinuata
Hesperis armena
Leavenworthia alabamica
Blennodia pterosperma
Leptaleum filifolium
Hesperis steveniana
Farsetia aegyptiaca
Matthiola lunata
Hesperis podocarpa
Matthiola
odoratissima
Matthiola
codringtonii
Matthiola taurica
obovata
Matthiola
tenera
Matthiola tatarica Matthiola
Moricandia moricandioides
Matthiola trojana
Matthiola caspica
Hesperis schischkinii
Eruca strum l ittoreu m
Diplotaxis gorga densi s
Mathewsia incana
Leavenworthia exigua
Malcolmia micrantha
Matthiola maroccana
Matthiola aspera
Bra ssi ca tardarae
Farset ia stylosa
Erysi mum maj ellense
Erysimum ca ndicum
Hesperis dinarica
Hesperis laciniata
Matthiola livida
Matthiola
jurtina
Matthiola
perennis
Biscu tella raphanifolia
Bunias eruca go
Bra ssica tyrrh ena
Erysi mum f orrestii
Erysimum
rip
haeanum
Erysimum
h mum
andel-mazze
ttii d uria ei
Erysi
mum
aurantiacum
ErysiErysi
mum
pseudorhaeticum
Erysimum ron dae
Erysimum cheiri
Diceratella elliptica
Parrya subsiliquosa
Matthiola longipetala
Moricandia
arvensis
Erysimum p erenne
Erysimum
llisparsum
Erysimum co
merxmu
elleri syl vest re
Erysimum
mum
a mmophilum
ErysiErysi
mum
j ugicola
Chorispora songarica
Brassi ca baldensis
Morettia philaeana
Malcolmia graeca
Coincya wrig htii
Coincya monensis. nevadensis
Erysimum b elvederense
Erysimum med iohispanicum
Brassica insularis
Conrin gia orie ntalis
Erysi mum p ycnophyllum
Bra ssi ca rupestris
Dithyrea maritima
Matthiola ghorana
Matthiola incana
Lepidium si symbrio ides
Lepidium pseudopapillosum
Dryopetalon stenocarpum
Lepidium alluaudii
Phlegmatospermum eremaeum
Iberis halophita
Dryopetalon runcinatum
Hymenolobus procu mbens
Iberis procumbens
Iberis saxatilis.longistyla
Iberis amara
Pennellia tricornuta
Brayopsis calycina
Iberis sempervirens
Hornu ngia petraea
Lepidium tran svaalense
Microlepidium alatum
Lepidium pseudohysso pifolium
Lepidium pseudotasman icum
Lepidium sa gittulatum
Lepidium p seudoruderale
Lepidium nesophilum
Lepidium reko huense
Lepidium boelcke anum
Brayo psis monimocalyx
Lepidium mon oplocoides
Lepidium p apillosum
Pennellia micrantha
Lepidium so landri
P
Microt hlasp i natolicum
Lepidium mue lleriferdi nandi
-0.2
Lepidium oxyt rich um
Lepidium hypenantion
Lepidium o ligodontum
Lepidium hysso pifolium
Iberis semperflorens
Iberis saxatilis.cinerea
Iberis pectinata
Asch erson iodoxa cach ensis
Macropodium
Macropodium
pterospermum
nivale
Iberis gibraltarica
Lepidium
d epressu
m ii
Lepidium
parod
Lepidium
basu
ticum
Lepidium
ca
pense
Lepidium
suluense
Lepidium
fasci
culatum
Lepidium
asch
erson ii
Lepidium rah meri
Lepidium p seudodidymum
t andilense
Lepidium
pedersen
iii
Lepidium
h ickenii
Lepidium
rhytauricu
idocarpum
Lepidium
burkarti
Lepidium africa num
Lepidium
graci
Lepidium
latum
Lepidium
j ohnstonii
Lepidium
argentinum
Coronopus
integrif
olius
Lepidium
sa
ntacruze
nsisle
Lepidium
myri
anthum
Lepidium
st
ucke
rtianum
f ilisegmentum
Lepidium
sp
icatum
Lepidium
rei ch ei
IberisIberis
carnosa.granatensis
carnosa.carnosa
Iberis saxatilis.saxatilis
Clypeola aspera
m
M
m
-0.2
-0.1
0.0
0.1
m
0.2
NMDS1
783
784
Figure 1. Plasticity-mediated floral disparity. (A) Floral morphospace of the Brassicaceae,
785
showed as the projection of 31 traits recorded in 3140 species onto two NMDS axes. The position
786
of the spring and summer phenotypes of Moricandia arvensis is linked by a thick lilac dashed line.
787
We have also indicated the movements across this morphospace of several species changing
788
their phenotypes due to floral colour polymorphism (black lines), single mutations in floral colour
789
(blue lines), changes in breeding systems (orange lines), changes in gender expression (green
790
lines), homeotic mutations (brown lines), and plasticity (lilac lines). Numbers matching species
791
are as follow: 1-Lobularia maritima; 2-Raphanus raphanistrum; 3-Matthiola incana; 4-Mathiola
792
fruticulosa; 5-Erysimum cheiri; 6-Cakile maritima; 7-Matthiola lunata; 8- Marcus-kochia littorea; 9-
793
Hesperis matronalis; 10- Hesperis laciniata; 11-Parrya nudicalis; 12-Streptanthus glandulosus;
794
13- Eruca vesicaria; 14- Capsella bursa-pastoris; 15-Hormathophylla spinosa; 16- Brassica
795
napus; 17- Cardamine hirsuta; 18- Lepidium sisymbrioides; 19-Lepidium solandri; 20-Arabidopsis
796
thaliana; 21-Boechera stricta; 22-Leavenworthia stylosa; 23-Leavenworthia crassa; 24-
797
Pachycladon stellatum; 25- Pachycladon wallii; 26-Cardamine kokairensis; 27-Brassica rapa. (B)
798
Shepard plot showing the goodness of fit of the NMDS ordination. (C) Moricandia arvensis in
799
spring. (D) Moricandia arvensis in summer. (E) Magnitude of floral disparity between different
800
taxonomic levels of Brassicaceae species. The number above each boxplot shows the number of
801
disparities per level. We have compared this value with the disparity between spring and summer
24
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
802
phenotypes of M. arvensis (this comparison with boxplots in red is statistically significant at P <
803
0.05, in orange is marginally significant at P < 0.1, and in grey is non-significant).
804
805
25
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
806
807
808
Figure 2. Phylogenetic-mediated floral divergence. (A) Floral phylomorphospace using the
809
supertree that includes 1876 Brassicaceae species. (B) Phylomorphospace considering only the
810
eight Moricandia species, using the Perfectti et al.'s phylogeny (phylogeny # 1 in Table S8). (C)
811
Floral disparity to the nearest ancestor, according to the supertree and 18 time-calibrated
812
phylogenies (phylogeny codes in Table S8). We show the disparity between the two M. arvensis
813
phenotypes and their direct ancestor (spring: lilac dots; summer: white dots) in those phylogenies
26
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
814
that include Moricandia. We also show the disparities to their direct ancestors of those
815
Brassicaceae species included in time-calibrated phylogenies of more than 45 species.
816
817
27
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
818
a
1
2
3
Niches
4
5
b
6
7
8
NOCTURNAL MOTH
AUTOGAMY
LARGE WASP
SPIDER
LARVA
GRASSHOPPER
EARWIG
LACEWING
SNAKEFLY
BIRD
HONEYBEE
SHORT-TONGUED LARGE BEE
SHORT-TONGUED MEDIUM-SIZED BEE
SHORT-TONGUED SMALL BEE
SHORT-TONGUED EXTRA LARGE BEE
SHORT-TONGUED EXTRA SMALL-BEE
LARGE HOVERFLY
SMALL HOVERFLY
SMALL BEEFLY
LARGE FLY
SMALL FLY
LONG-TONGUED FLY
LARGE MOTH
SMALL MOTH
POLLEN WASP
HAWKMOTH
LARGE BEEFLY
LONG-TONGUED LARGE BEE
LONG-TONGUED MEDIUM-SIZED BEE
LONG-TONGUED EXTRA LARGE BEE
SMALL BEETLE
LARGE BEETLE
SMALL DIVING BEETLE
BUG
SMALL BUG
APHID
MITE
SPRINGTAIL
SMALL WASP
THRIPS
LARGE BUTTERFLY
SMALL BUTTERFLY
SMALL ANT
LARGE ANT
1.0
0.2
0.0
0.1
0.0
-0.1
-0.2
-0.2
-0.1
0.0
0.1
0.2
c
Rytidocarpus moricandioides
Niches
Main pollinators
Niches
Main pollinators
Moricandia foetida
0.97
Moricandia rytidocarpoides
0.91
Moricandia moricandioides
1.00
0.97
Moricandia nitens
1.00
1
5
2
6
3
7
4
8
Moricandia suffruticosa
1.00
Moricandia spinosa
1.00
Moricandia arvensis
Eruca foleyi
1.00
1.00
Eruca vesicaria
Eruca pinnatifida
819
820
Figure 3. Plasticity-mediated changes in pollination niches. (A) Outcome of the modularity
821
analysis showing the number of pollination niches inferred, the among-niche differences in
822
relative frequency of each pollinator functional group, and the pollinator functional groups defining
823
the niches (n = 511 Brassicaceae species). (B) Morphospatial distribution of the eight pollination
824
niches detected in Brassicaceae. Insect silhouettes were drawn by Divulgare (www.divulgare.net)
825
under a Creative Commons license (http://creativecommons.org/licenses/by-nc-sa/3.0). (C)
826
Estimate of the ancestral pollination niche of the Moricandia lineage using a stochastic character
827
mapping inference analysis. The numbers underneath each ancestral node indicate the posterior
828
Bayesian probability of belonging to pollination niche 5.
829
830
28
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
831
832
833
Figure 4. Plasticity-mediated floral convergence. Convergent lineages crossing into the region
834
of the morphospace delimited by the pollination niche of the M. arvensis during spring (the shade
835
convex hull) according to (A) Smith & Brown's phylogeny, (B) Gaynor et al.'s phylogeny, and (C)
836
Huang et al.'s phylogeny (phylogenies 2-4, respectively, in Table S8). Convergent lineages
837
crossing into the region of the morphospace delimited by the pollination niche of the M. arvensis
838
during summer (the shade convex hull) according to (D) Smith & Brown's phylogeny, (E) Gaynor
839
et al.'s phylogeny, and (F) Huang et al.'s phylogeny. Red arrows indicate the plasticity-mediated
840
convergence, blue arrows the convergence events of the other lineages. The small purple area in
841
all panels is the region of the floral morphospace that includes the lineages that have converged
842
with the entire Moricandia clade according to each time-calibrated phylogeny.
843
844
29
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
SI FIGURES
Figure S1. Association among the 31 pollination traits of 3140 Brassicaceae species. Trait
vectors represent the Spearman correlations, with the length and direction indicating the
relationship with composite NMDS axes.
Petal length
Petal carotenoids
Sepal length
0.2
Long stamens length
Short stamens length
Petal colour CIELAB
Tetradynamous
condition
Petal limb length
0.1
Concealed nectaries
Number Plant
of stamens height Relative petal
attractiveness
Stamen
Bullseyes dimorphism
Sepal colour CIELAB
Petal veins
Petal
anthocyanins
Flower display
0.0
Horizontal corolla
Coloured sepals
Overlapped petals
Stamen exsertion
Multilobed petals
Inforescence architecture
Number of symmetry axes
Sepal hue
Visible anthers
-0.1
Asymmetric petals
Visible sepals
Petal hue
-0.2
Apetalous flower
-0.2
-0.1
0.0
0.1
0.2
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
SI TABLES
Table S1. Fitting of the floral traits onto the NMDS vectors.
Floral traits
NMDS1
NMDS2
r2
P value
1
Plant height
-0.20147
0.97949
0.1126
0.001
2
3
4
5
Flower display size
Inflorescence architecture
Presence of apetalous flowers
Number of symmetry axes of the corolla
0.80044
0.94742
0.36770
0.66735
0.59942
-0.32001
-0.92994
-0.74474
0.0415
0.0641
0.1452
0.1121
0.001
0.001
0.001
0.001
6
7
8
9
10
Orientation of dominant symmetry axis of the corolla
Corolla with overlapped petals
Corolla with multilobed petals
Corolla with visible sepals
Petal length
0.98547
-0.98142
-0.45075
0.70871
-0.55200
0.16987
-0.19188
-0.89265
-0.7055
0.83385
0.2650
0.0685
0.0110
0.2729
0.6287
0.001
0.001
0.001
0.001
0.001
11
12
13
14
15
Sepal length
Asymmetric petals
Petal limb length
Length of long stamen
Longeth of short stamen
-0.47963
-0.49289
-0.67904
-0.48773
-0.42415
0.87747
-0.87009
0.73410
0.87300
0.90559
0.5594
0.0604
0.4482
0.4915
0.4029
0.001
0.001
0.001
0.001
0.001
16
17
18
19
20
Herkogamy
Herkogamy category
Visible anthers
Excerted stamens
Number of stamens
-0.78612
-0.62172
0.76256
0.29511
-0.28006
0.61808
0.78324
-0.64691
-0.95546
0.95998
0.1671
0.3864
0.1526
0.0033
0.1182
0.001
0.001
0.001
0.009
0.001
21
22
23
24
25
Concealed nectaries
Petal carotenoids
Petal anthocyanins
Presence of bulleyes
Presence of veins in the petals
-0.72601
0.61077
-0.98947
-0.84653
-0.94487
0.68768
0.7918
0.14476
0.53235
0.32746
0.4101
0.7264
0.5757
0.2654
0.3343
0.001
0.001
0.001
0.001
0.001
26
27
28
29
Coloured sepal
Relative attractiveness of petals versus sepals
Petal hue
Petal colour as b CIELAB
0.99357
-0.00049
0.60720
0.75326
-0.11318
0.99990
-0.79455
0.65772
0.0039
0.1001
0.2096
0.7232
0.002
0.001
0.001
0.001
0.61109
0.87412
-0.79156
0.48571
0.0791
0.5605
0.001
0.001
30 Sepal Hue
31 Sepal colour as b CIELAB
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S2. Disparity, calculated as the Euclidean distance in the family-wide floral
morphospace, between each of the 38 morphs included in our dataset (see
Supplementary Data 2 for details and references) and their respective wild types.
Type of polymorphism
Breeding system
Breeding system
Breeding system
Breeding system
Colour mutant
Colour mutant
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Flower colour polymorphism
Gender dimorphism
Gender dimorphism
Gender dimorphism
Gender dimorphism
Gender dimorphism
Gender dimorphism
Homeotic mutant
Homeotic mutant
Homeotic mutant
Homeotic mutant
Phenotypic plasticity
Phenotypic plasticity
Species
Brassica napus
Brassica rapa
Cardamine kokairensis
Leavenworthia crassa
Brassica napus
Moricandia arvensis
Boechera stricta
Boechera stricta
Cakile maritima
Eruca vesicaria
Erysimum cheiri
Erysimum cheiri
Hesperis laciniata
Hesperis matronalis
Hormathophylla spinosa
Leavenworthia stylosa
Lobularia maritima
Marcus-kochia littorea
Matthiola fruticulosa
Matthiola incana
Matthiola lunata
Parrya nudicaulis
Raphanus raphanistrum
Raphanus raphanistrum
Raphanus raphanistrum
Streptanthus glandulosus
Hormathophylla spinosa
Hormathophylla spinosa
Lepidium sisymbrioides
Lepidium solandri
Pachycladon stellatum
Pachycladon wallii
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana
Capsella bursapastoris
Cardamine hirsuta
Cardamine hirsuta
Morph
cleistogamous mutant
female sterility mutant
cleistogamous mutant
Outcrosser morph
white mutant
white mutant
pink morph
purple morph
white morph
white morph
purple cultivar
white cultivar
white morph
white morph
white morph
white morph
deep purple cultivar
light pink morph
greenish morph
white cultivar
white morph
white morph
white morph
yellow morph
pink morph
white morph
female morph
male morph
female morph
female morph
female morph
male morph
AGAMOUS mutant
APETALA1 mutant
APETALA3 mutant
Spe mutant
plastic change in stamens number
plastic change in petal number
NMDS
0.035856865
0.133332180
0.111696867
0.015771684
0.173001555
0.149565069
0.060580070
0.054429426
0.016547552
0.082257145
0.073997237
0.026460490
0.069557518
0.094873544
0.101607789
0.066269050
0.090407642
0.019542946
0.008349920
0.138357728
0.079964493
0.115226060
0.082072459
0.032685632
0.082778860
0.014907493
0.035783402
0.025226337
0.067913758
0.065685257
0.014244744
0.059320935
0.001052532
0.119617731
0.102445400
0.051187659
0.010624208
0.060755859
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S3. Floral disparity of each species of Moricandia from the most recent common
ancestor (MRCA) of the genus and from the direct ancestor of each species.
Species
Moricandia foetida
Moricandia moricandioides
Moricandia nitens
Moricandia rytidocarpoides
Moricandia sinaica
Moricandia spinosa
Moricandia suffruticosa
Moricandia arvensis spring phenotype
Moricandia arvensis summer phenotype
Disparity to MRCA
0.039566021
0.059142993
0.041727403
0.025809374
0.027589330
0.019579372
0.063884437
0.080840848
0.195061288
Disparity to direct
ancestor
0.13987379
0.03730920
0.07347209
0.10503623
0.10550411
0.20959717
0.20700167
0.02385532
0.28741584
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S4. Significance of the Mantel tests checking for spatial autocorrelation across
the morphospace of the pollinator functional groups. Due to the small abundance of
some pollinators, the original 43 functional groups have been pooled in 26 main
functional groups.
Functional Groups
Ant
Autogamy
Bug
Butterfly
Hawkmoth
Hoverfly
Large beefly
Large beetle
Large fly
Large wasp
Long tongued fly
Long tongued large bee
Long tongued medium-sized bee
Moth
Nocturnal moth
Other
Pollen wasp
Small beetle
Small diving beetle
Small fly
Small wasp
Short tongued large bee
Short tongued medium-sized bee
Short tongued small bee
Short tongued extra small bee
Thrips
Mantel R
0.047
0.257
0.032
0.089
0.054
0.072
0.043
0.046
0.052
0.053
0.092
0.242
0.051
0.039
0.222
0.018
0.026
0.012
0.003
0.112
0.041
0.065
0.012
0.073
0.020
-0.014
p value
0.055
0.001
0.192
0.001
0.035
0.003
0.079
0.063
0.044
0.048
0.001
0.001
0.041
0.113
0.001
0.497
0.313
0.613
0.899
0.001
0.112
0.004
0.590
0.001
0.454
0.758
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S5. Diferences between the two Moricandia arvensis phenotypes in the
visitation frequency (both in absolute number of insects and in proportion of visits) of
every pollinator functional group. Fifteen censuses of 1 hr and two researchers per
phenotype.
Pollinator functional group
Hawkmoth
Honeybee
Large beefly
Large beetle
spring
phenotype
summer
phenotype
spring
phenotype
(proportion)
summer
phenotype
(proportion)
91
40
309
30
0
0
72
40
0.036
0.016
0.124
0.012
0.000
0.000
0.148
0.082
280
38
8
1131
226
66
0
7
5
0
0.112
0.015
0.003
0.453
0.090
0.135
0.000
0.014
0.010
0.000
Small beefly
Small beetle
Small butterfly
Small diving beetle
Small fly
6
21
11
25
12
0
8
0
12
0
0.002
0.008
0.004
0.010
0.005
0.000
0.016
0.000
0.025
0.000
Small hoverfly
Small moth
Short tongued large bee
Short tongued medium-sized bee
Short tongued small bee
49
2
89
36
78
37
7
3
0
207
0.020
0.001
0.036
0.014
0.031
0.076
0.014
0.006
0.000
0.424
Short tongued extra small bee
Thrips
1
15
0
24
0.000
0.006
0.000
0.049
Large butterfly
Large fly
Large hoverfly
Long tongued large bee
Long tongued medium-sized bee
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S6. Outcome of the analyses to test the occurrence of floral convergence among
plants from niches 3 and 5. Angle is the mean theta angle between all species belonging to
the same niche. Angle/time is the angle divided by time distance. The significance of these
angles has been found by comparing with a null model consisting in shuffling each niche 1,000
times across the tree tips and calculating a distribution of random angle. C1 measures the
proportion of phenotypic distance closed by evolution, ranging from 0 to 1 (where 1 indicates
complete convergence). C2 is the raw value of the difference between the maximum and
extant distance between the lineages. C3 is C2 scaled by the total evolution (sum of squared
ancestor-to-descendant changes) between the two lineages. C4 is C2 scaled by the total
evolution in the whole clade. The significance of C1-C2, was evaluated by running 1000
simulations for each comparison using Brownian-Motion models. Wheatleaf is the ratio of the
mean (penalized) distances between all species to the mean (penalized) distances between
allegedly convergent species. Significance found by running 2000 bootstrapping simulations. In
bold, significant values.
Phylogenies
Niche 3
Angle
Angle/time
C1
C2
C3
C4
Wheatleaf
Niche 5
Angle
Angle/time
C1
C2
C3
C4
Wheatleaf
Smith & Brown 2018
Value
p
Gaynor et al. 2018
Value
p
Huang et al. 2019
Value
p
80.587
2.350
0.373
0.104
0.141
0.003
0.830
0.008
0.719
0.000
0.000
0.000
0.720
0.986
79.431
1.645
0.472
0.142
0.166
0.002
0.940
0.002
0.397
0.000
0.000
0.000
0.700
0.715
64.930
4.023
0.415
0.104
0.219
0.008
1.060
0.055
0.815
0.000
0.000
0.000
0.600
0.028
70.093
1.393
0.356
0.110
0.128
0.003
1.120
0.002
0.021
0.000
0.000
0.000
0.727
0.673
73.491
1.783
0.472
0.142
0.166
0.002
1.170
0.002
0.745
0.000
0.000
0.000
0.700
0.094
58.313
2.474
0.240
0.075
0.118
0.006
0.920
0.049
0.011
0.000
0.000
0.000
0.545
0.978
Table S7. Outcome of the analyses testing for morphological convergence between the Moricandia clade and the rest of clades included in each time-calibrated
phylogeny. Clade size is the number of species within the Moricandia clade. θreal is the mean angle over all possible combinations of pairs of species taking one species per
clade. θace is the mean angle between ancestral states between each pairs of clades. distmrca is the patristic distance (sum of brach length) between the most recent
common ancestors of each pair of clade. We indicate the congervent clades and the pollination niches of each species included in the convergent clades. In red Moricandia
clades including Moricandia arvensis spring phenotype. Tribes (E= Erysimeae, A= Anchonieae, C=Cardamineae, M=Malcolmieae, An=Anastaticeae).
θreal/distmrca θace+θreal/ θace+θreal/
Convergent clades
Tribe
Moricandia Clade
Clade
θreal
θace
distmrca
θreal/
p-value
clade
2
size
distmrca
distmrca
distmrca
p-value
Smith & Brown's phylogeny
253
347
7
15.200
4.420 124.236
0.122
0.058
0.158
0.012
Erysimum bicolor/ scoparium)
E
254
347
5
19.035
5.389 129.718
0.147
0.058
0.188
0.016
Erysimum bicolor/ scoparium
E
255
256
256
256
5,5
5,5
4
2
2
2
22.601
6.180
12.950
8.543
6.331 133.342
7.281 133.538
2.109
59.810
13.786
49.285
0.169
0.046
0.217
0.173
0.052
0.026
0.061
0.066
0.217
0.101
0.252
0.453
0.019
0.005
0.018
0.045
Erysimum bicolor/ scoparium
Erysimum bicolor/ scoparium
Matthiola clade
Cardamine penthaphyllo/ pratensis
E
E
A
C
5,5
5,5
6,1
3,7
256
405
256
335
257
347
258
347
Gaynor et al.'s phylogeny
2
2
2
2
8.616
28.715
39.021
5.613
1.048
44.577
33.529 128.518
6.003 133.462
4.410 124.383
0.193
0.223
0.292
0.045
0.068
0.077
0.103
0.012
0.217
0.484
0.337
0.081
0.022
0.049
0.015
0.002
Malcolmia maritima— Marcus-kochia ramosissima
Erysimum popovii/ bastetanum/ semperflorens
Erysimum bicolor/ scoparium
Erysimum bicolor/ scoparium
M/An
E
E
E
5,7
5,5,6
5,5
5,5
481
334
479
334
479
333
Huang et al.'s phylogeny
143
83
2
2
2
10.943
9.357
12.809
17.832
12.654
14.978
78.194
81.141
81.151
0.140
0.115
0.158
0.052
0.052
0.070
0.368
0.271
0.342
0.037
0.033
0.049
Erysimum bicolor/ scoparium
Erysimum bicolor/ scoparium
Erysimum lagascae/ rondae
E
E
E
5,5
5,5
5,3
2
4.960
0.985
23.966
0.207
0.023
0.248
0.001
Erucaria clade
B
3,5
2
2
2
2
2
7.094
6.651
9.229
11.634
9.383
0.554
40.317
1.876
12.691
12.437
22.049
18.008
23.466
24.281
24.007
0.322
0.369
0.393
0.479
0.391
0.041
0.046
0.066
0.074
0.076
0.347
2.608
0.473
1.002
0.909
0.002
0.170
0.003
0.026
0.029
Erucaria clade + Cakile clade
Erucaria clade + Cakile clade + Eremophyton chevallieri
Cakile clade
Zilla clade
Zilla clade + Foleyola billotii
143
143
143
143
143
347
347
316
375
Niche
82
81
84
86
85
B 3,3,3,5
B 3,3,3,5,5
B
3,3
B
5,5
B
3,5,5
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S8. Description of floral traits related to pollinator attraction used to generate
the floral morphospace in Brassicaceae. Pollinators respond to the variability of
numerous phenotypic traits of plants, and the magnitude of their response shapes the
reproductive success of the plants. We estimated for each plant included in our data set
the values of several important floral traits.
1) Plant height. Plant height has strong direct and indirect effects on plant fitness in many
Brassicaceae. The assessment of plant height for a large number of plant species is not
possible without accurate ecological studies. In addition, the information on plant size in
general (and plant height in particular) appearing in the floristic catalogues is limited and
most time very vague. For this reason, we decided to consider this variable as semiquantitative, with three levels:
0 = This group includes plants with a prostrate life habit. Plants belonging to this group
are those with a cushion shape, displaying flowers located very close to the ground and
that thereby can be accessed both by flying and crawling insects (ants, springtails, mites,
etc.).
1 = This group includes plants of intermediate size. We included in this group those plants
shorter than 50 cm. This threshold is appropriate because it teases apart medium-sized
species from those species with a large size. Many pollinators have a specific flight pattern
with changes in flight zones occurring around this threshold. Within this group, there are
also subshrub species with stunted growth habit.
2 = This group includes plants of large size. We included in this group those plants taller
than 50 cm. These are plants particularly big, usually log-lived and sometimes woody
species.
(2) Flower display size. The number of flowers produced per individual plant has strong
direct and indirect effects on plant fitness in most Brassicaceae species. As occurring with
plant height, the assessment of floral display size for a large number of plant species is not
possible without accurate ecological studies. In addition, the information on flower
number per individual appearing in the floristic catalogues is limited and most time very
vague. For this reason, we decided to consider this variable as semi-quantitative, with
three levels:
0 = This group includes species with few flowers per individual (pauciflorous), usually less
than 50 flowers per individual.
1= This group includes species with medium number to many flowers per individuals,
usually between 50 and 1000 flowers per individual.
2 = This group includes species mass-flowering species, usually with more than 1000
flowers per individual.
(3) Inflorescence architecture. The configuration of flowers along the flowering stems
and the inflorescence architecture have been shown to affect the attractiveness and
foraging behaviour of pollinators in many angiosperm groups since long time. In
Brassicaceae three main types of inflorescences can be distinguished:
0 = Inflorescences where flowers are arranged in solitary. In this species, flowers do not
form a dense inflorescence but are solitary usually at the end of the flowering stems.
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
1 = Inflorescences where flowers are arranged in racemes. A simple inflorescence in which
the main axis is indeterminate. This is the most frequent type of inflorescence in
Brassicaceae.
2 = Inflorescences where flowers are arranged in corymbs. This is a special case of a
panicle where flowers lie in a single plane. Panicles are determinate compound
inflorescences in which branching does not occur from the axils of prophylls.
(4) Presence of apetalous flowers. Several species from some Brassicaceae genera,
especially Lepidium and Rorippa, and to a lesser extent Romanschulzia, Clypeola,
Cardamine and other minor genera, produce flowers without petals. We classified this
floral trait as presence (1) or absence (0) of apetalous flowers.
(5) Number of symmetry axes of the corolla. Flower symmetry is an important trait in
flowering plants. The Brassicaceae flower is defined as a cruciform, actinomorphic or
radial flowers with many symmetry axes. However, it is widely acknowledged that some
genera such as Iberis or Teesdalia produce monomorphic or actinomorphic flowers. The
number of symmetry axes is even greater in some species. We have distinguished four
groups based on number of symmetry axes:
0 = This group includes plants with flowers having no symmetry axis, like many species of
Matthiola, some Hesperis,
1 = This group includes plants bearing flowers with one symmetry axis or actinomorphic
flowers. In this group we included Iberis, Teesdalia, and several species of Noccaea,
Thlaspi, etc.
2 = This group includes plants bearing flowers with two symmetry axes or dissymmetric
flowers. This is probably the most abundant group, including most common species of
Brassicaceae, like Erysimum, Brassica, Diplotaxis, etc.
4 = This group includes plants bearing flowers with four or more symmetry axes or
polysymmetric flowers. This group, including common species of Brassicaceae, like
Lepidium, some Erysimum, many Heliophila, many Sisymbrium, etc.
(6) Orientation of dominant symmetry axis of the corolla. In Brassicaceae, most
flowers orientate vertically. Thereby, we classified this floral trait as horizontally- (1) or
vertically- (0) orientated flowers.
(7) Corolla with overlapped petals. Much like flower symmetry, the presence of
overlapped petals and rounded corollas affect fitness in several plant groups, including
some Brassicaceae species by mediating the attractiveness of the flowers and the
behaviour of pollinators. We classified this floral trait as corolla with overlapped petals (1)
or with non-overlapped petals (0).
(8) Corolla with multilobed petals. In Brassicaceae petal lobes is not widespread,
although it is frequent in some clades such as Schizopetalon, Berteroa, Dryopetalon. We
classified this floral trait as corolla with multilobed petals (1) or without them (0).
(9) Corolla with visible sepals. Sepals play an important role in the pollination of many
plant species. Some plant species, including Brassicaceae, have extended sepals that are
visible from the top of the corolla. These visible petals may have important consequences
on the behaviour of some pollinators, indirectly influencing the pollination success of the
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
flower. We scored this floral trait as corolla with visible sepals from the top of the corolla
(1) or not (0).
(10) Petal length. Different studies have found a significant association between the
length of flower petals and the behaviour of pollinators, by increasing corolla size and
attractiveness or the floral attraction surface. As a consequence, it has been frequently
proven the occurrence of a significant effect of petal length and flower size on the
efficiency of pollination. We included in the data set the length of the petal in mm of each
plant species. For this, we retrieved from the literature the description of the petal length,
and calculated the mean of the values appearing in that description.
(11) Sepal length. In Brassicaceae the length of the sepals is positively correlated with the
length of the corolla tube and the amount of nectar produced by the flowers. We included
in the data set the length of the sepals in mm of each plant species. As in traits 10, we
retrieved from the literature the description of the sepal length, and calculated the mean
of the values appearing in that description.
(12) Asymmetric petals. Brassicaceae is characterized for bearing four symmetric petals.
However, some species exhibit corollas with asymmetric petals, a character considered a
morphological novelty. Presence of asymmetric petals causes corollas to show
zygomorphy. This character, by affecting in an extreme way the number of symmetry axes,
have larges effects on pollinator preference, pollination efficiency and reproduction
success. We scored this floral trait as corolla with asymmetric petals (1) or not (0).
(13) Petal limb length. The limb of the petal is the showy part that directly attracts
pollinators. We included in the data set the length of the petal limb in mm of each plant
species. For this, we retrieved from the literature the description of the petal length, and
calculated the mean of the values appearing in that description.
(14) Length of long stamens. Brassicaceae has a tetradynamous androceum, with an
outer whorl of two short stamens and an inner whorl of four long stamens. The length of
the long stamens has been proven to affect pollinator visitation rate and effectiveness,
having a strong effect on pollen removal and male fitness. We included in the data set the
length of the long stamen in mm of each plant species as appearing in the literature.
(15) Length of short stamens. Short stamens may function in outcrossing Brassicaceae to
reduce pollen depletion with high rates of pollinator visitation. In self-compatible, short
stamens may favour delayed autogamy. In addition, short stamens may also affect
pollinator visitation rate and effectiveness, having potential effect on pollen removal and
male. We included in the data set the length of the short stamen in mm of each plant
species as appearing in the literature.
(16) Stamen dimorphism. The difference in length between long and short stamens,
hereinafter herkogamy, is related in Brassicaceae with pollinator attraction and evolution
of selfing syndrome. We included this trait by estimating the length difference between
long and short stamens from the data obtained in the literature.
(17) Tetradynamous conditions. In addition, we classified all Brassicaceae included in
our dataset as having an androecium with all stamens equally long (0), slightly
tetradynamous (1), normal tetradynamous condition (2) and strong tetradynamous
condition (3). We used the classification appearing in the floral and formal description of
the species.
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
(18) Visible anthers. Most species of Brassicaceae have anthers visible from outside the
corolla during anthesis, which ease the magnitude of pollen removal by flower visitors.
However, species of some genera (Matthiola, Hesperis, Farsetia, etc.) have stamens well
hidden within the corolla tube and imperceptible from outside, a trait that difficult shorttongued insects to collect pollen. We scored this floral trait as corolla with visible anthers
(1) or not (0).
(19) Exserted stamens. In some Brassicaceae the filaments are very long, causing
stamens to be highly exserted. Stamens exsertion influences the behaviour and abundance
of certain pollinators, shaping pollinator-mediated selection through male fitness. We
scored this floral trait as non-exserted stamens (0) slightly exserted stamens (1) and
strongly exserted stamens (2).
(20) Number of stamens. The basic number of stamens per Brassicaceae flower is six.
However, departure from this number is frequent in some lineages such as Lepidium or to
a lesser extent Cardamine or Alyssum, where some species bear 2, 4 or 5 stamens. In
addition, some species of the genus Megacarpea have flowers with 9 or more stamens. We
included for each species in the dataset the number of stamens indicated in the literature.
(21) Concealed nectaries. Some Brassicaceae species produce nectar that is concealed in
the bottom of long corolla tubes, whereas other species bearing bowl-shaped flowers
produce nectar that is freely exposed an easily accessible. This trait may have important
consequences for the interaction with pollinators. We scored this floral trait as corolla
with concealed nectaries (1) or not (0).
(22) Petal carotenoids. Flower colour is a crucial visual cue used by pollinators to locate
flowers. In the Brassicaceae, there are numerous studies highlighting the role of flower
colour in pollinator attraction and plant reproduction. Petal colour is mainly determined
by the presence of pigments; we thereby decided to include the presence or absence of
floral pigments in our dataset. Yellow colour is produced in Brassicaceae by the
accumulation of carotenoids. We scored this trait as the presence (1) or absence (0) of
petal carotenoids.
(23) Petal anthocyanins. In the Brassicaceae, species with pink, lilac, blue, purple, orange
and red petals are caused by the accumulation of anthocyanins. We scored this floral trait
as the presence of petal anthocyanins (1) or absence (0).
(24) Presence of bullseyes. Some flowers have circular patterns in the centre of the
corolla called bullseyes that is involved in the attraction of pollinators. Bullseyes may be
visible to human vision or invisible due to its absorbance in the ultraviolet region of the
light spectrum; we considered only the first ones as is the information provide in the
consulted Floras. We scored this floral trait as corolla with (1) or without (0) bullseyes.
(25) Presence of veins in the petals. In the Brassicaceae, some species may show petals
with prominent veins having a different colour from the rest of the petals. The presence of
coloured veins in the petals may function as nectar guides, providing visual orientation
directing the pollinator to the central landing platform and the entrance to the flower. We
scored this floral trait as petals with (1) or without (0) veins.
(26) Coloured sepals. As commented in the trait 9, sepals may be involved in pollination
attraction in many species. Colouring sepals by accumulating anthocyanins or carotenoids
and may help flowers to differentiate from the green background. We scored this floral
trait as coloured sepals (1) or green sepals (0).
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
(27) Relative attractiveness of petals versus sepals. In some species of the
Brassicaceae, the sepals are bigger and more attractive than the petals. This occurs
frequently in some genera such as Streptanthus, Roripa, Lepidium and Heliophila. We
scored this floral trait as (1) when petals are more attractive than sepals or (0) in the
opposite case.
(28) Petal hue. Although measuring flower colour with spectrophotometric methods are
recommended over methodologies based on human vision, obtaining reflectance data of
more than 3000 species widely distributed around the world is virtually unfeasible. We
designed a method that allows incorporating colour description in the Floras to generate
categorical variables. We used a modification of colour identification with reference
standards which are commonly used in comparative studies of flower colour and
generates relatively good estimates of flower colour variation. First, we used a subset of
200 species that we have digital photos taken with the same camera and similar light
conditions to prevent artificial colour modifications. The colour of petals was assigned to
the closest matching Munsell colour chip; the same person performed these measures in
order to avoid erroneous assignation due to inter-observer differences in colours
perception. A total of 24 colour types were identified covering shades of blue (2.5P7/6,
10PB7/6), lilac-purple (7.5P8/4, 7.5P6/8, 7.5P6/10, 7.5P4/10, 5P6/8, 5P8/4, 5P5/10),
pink (7.5RP8/4, 5RP6/10, 2.5RP5/10), yellow (5Y9/6; 5Y9/4, 5Y8.5/12), orange (5Y8/8,
2.5Y8/12, 2.5YR6/14), brown-bronze (10YR6/10, 5YR6/12, 10R5/8), green (2.5G5/5,
10GY6/8) and white (N9). We used spectral characteristics of Munsell colours to
transform the categorical colour data to semi-quantitative measures of colour. Hue is one
of the best colour descriptors for plant colourimetry; thus, we calculated hue values as the
wavelength at peak reflectance. In order to accommodate the Brassicaceae petal colour
information provided in the Floras to our 24 Munsell colour types, we generated ten
colour categories. The hue of each new colour category was calculated as the mean of the
hue values containing each category (i.e., among colour shades). In species with petal
colour variation, including petal colour polymorphism, we scored the more common petal
colour; if this information is not available, we assigned the colour derived of the presence
of floral pigments (anthocyanins, carotenoids or both). The values of the ten hue
categories are: 454.31 nm (blue), 503.55 nm (pink), 558.08 nm (lilac-purple), 572.46 nm
(yellow), 575.43 nm (pale yellow), 579.38 nm (yellow-orange), 592.74 nm (orange),
589.44 nm (brown-bronze), 546.10 nm (green) and 611.37 nm (white).
(29) Petal colour as b CIELAB. We also used a second parameter related to petal colour,
the “ b*” parameter of the CIE 1976 L*a*b*. In this colour space, b* dimension represent
values from -100 (blue colours) to 100 (yellow colours). This metrics is recommendable
for the analysis of flower colour, particularly in groups of plant species containing petals
with shades of yellow, as occurs in the Brassicaceae. b* values were obtained with the
same methodology explained in the previous trait (28). The values of the ten b* categories
are: -18.46 (blue), -4.77 (pink), -19.71 (lilac-purple), 45.03 (pale yellow), 80.1 (yellow),
80.45 (yellow-orange), 65.3 (orange), 52.02 (brown-bronze), 29.79 (green) and 0.00
(white).
(30) Sepal hue. Sepals of Brassicaceae species are sometimes coloured, differing from the
common green. As already mentioned above for traits 9, sepals play an important role in
the pollination of many plant species. We used the same method and hue values detailed
in the trait 28 to score the sepal colour as hue category.
(31) Sepal colour as b CIELAB. For the same reasons mentioned above, we decided to
include this trait because of the effect it can have on attracting pollinators. We used the
same method and values detailed in the trait 29 to score the sepal colour as “b*”
parameter of the CIE 1976 L*a*b*.
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S9. List of the phylogenies retrieved from the online repositories and from the
literature to built up the Brassicaceae supertree. Within brackets appears the number
of species included in the analysis of disparity
Code
Species
Dated Rooted Focal taxa
Phylogenies including Moricandia
1
15 [8] YES
YES
Moricandia
2
273 [255] YES
YES
3
1508 [248] YES
YES
4
195 [163] YES
YES
Brassiceae
Time-calibrated phylogenies with more than 45 spp
5
84 [48] YES
YES
Euclideae
6
130 [124] YES
YES
7
316 [208] YES
YES
8
165 [109] YES
YES
Alysseae
9
46 [26] YES
YES
Anchonieae
10
265 [265] YES
YES
Arabidae
11
84 [77] YES
YES
Boechereae
12
160 [126] YES
YES
Cardamineae
13
57 [23] YES
YES
Chorisporeae
14
51 [28] YES
YES
Coluteocarpaeae
15
110 [89] YES
YES
Erysimeae
16
75 [55] YES
YES
Euclidieae
17
56 [53] YES
YES
Heliophileae
18
139 [94] YES
YES
Lepidieae
19
130 [117] YES
YES
Thelypodieae
Time-calibrated phylogenies with less than 45 spp
20
10 YES
YES
Aethionemeae
Reference
Perfectti, F., Gómez, J. M., González-Megías, A., Abdelaziz, M., & Lorite, J. (2017).
Molecular phylogeny and evolutionary history of Moricandia DC (Brassicaceae). PeerJ, 5,
e3964.
Smith, S. A., & Brown, J. W. (2018). Constructing a broadly inclusive seed plant phylogeny.
American journal of botany, 105(3), 302-314
Gaynor, M. L., Ng, J., & Laport, R. G. (2018). Phylogenetic structure of plant communities:
are polyploids distantly related to co-occurring diploids?. Frontiers in Ecology and
Evolution, 6, 52.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Chen, H., German, D. A., Al-Shehbaz, I. A., Yue, J., & Sun, H. (2020). Phylogeny of
Euclidieae (Brassicaceae) based on plastome and nuclear ribosomal DNA data. Molecular
Phylogenetics and Evolution, 153, 106940
Durka, W., & Michalski, S. G. (2012). Daphne: a dated phylogeny of a large European flora
for phylogenetically informed ecological analyses: Ecological Archives E093-214. Ecology,
93(10), 2297-2297
Walden, N., German, D. A., Wolf, E. M., Kiefer, M., Rigault, P., Huang, X. C., Kiefer, C.,
Schmickl R., Franzke A., Neuffer B., Mummenhoff, K., & Koch, M.A. (2020). Nested wholegenome duplications coincide with diversification and high morphological disparity in
Brassicaceae. Nature communications, 11(1), 1-12
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
21
9 YES
YES
22
30 YES
YES
23
10 YES
YES
24
5 YES
YES
25
19 YES
YES
26
6 YES
YES
27
8 YES
YES
28
27 YES
YES
29
16 YES
YES
30
8 YES
YES
31
29 YES
YES
32
13 YES
YES
33
41 YES
YES
34
17 YES
YES
35
24 YES
YES
36
25 YES
YES
37
23 YES
YES
38
11 YES
YES
39
13 YES
YES
40
6 YES
YES
41
34 YES
YES
42
5 YES
YES
43
5 YES
YES
44
8 YES
YES
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Anastaticeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Aphragmeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Asteae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Biscutelleae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Buniadeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Calepineae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Camelineae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Cochlearieae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Conringieae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Cremolobeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Crucihimalayeae Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Descurainieae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Dontostemoneae Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Eudemeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Eutremeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Halimolobeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Hesperideae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Hillielleae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Iberideae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Isatideae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Kernereae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Malcolmieae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Megacarpaeae
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Alyssopsideae
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
45
26 YES
YES
Microlepidieae
46
4 YES
YES
Notothlaspideae
47
5 YES
YES
Oreophytoneae
48
40 YES
YES
Physarieae
49
20 YES
YES
Schizopetaleae
50
23 YES
YES
Sisymbrieae
51
23 YES
YES
Smelowskieae
52
19 YES
YES
Thlaspideae
53
5 YES
YES
Turritideae
54
8 YES
YES
Yinshanieae
Non-time calibrated phylogenies
55
115 NO
YES
56
44 NO
NO
Erysimum
57
569 NO
YES
58
115 NO
NO
59
53 NO
YES
60
60 NO
YES
61
56 NO
YES
62
186 NO
YES
63
101 NO
YES
64
27 NO
NO
Microthlaspi
65
22 NO
YES
Alysseae
66
53 NO
YES
67
38 NO
YES
Thysanocarpus
Descurainia
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Huang, X.C., German, D.A. and Koch, M.A., 2020. Temporal patterns of diversification in
Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization
events. Annals of Botany, 125(1), pp.29-47.
Gómez, J. M., Torices, R., Lorite, J., Klingenberg, C. P., & Perfectti, F. (2016). The role of
pollinators in the evolution of corolla shape variation, disparity and integration in a highly
diversified plant family with a conserved floral bauplan. Annals of Botany, 117(5), 889904.
Gómez, J. M., Perfectti, F., Abdelaziz, M., Lorite, J., Muñoz-Pajares, A. J., & Valverde, J.
(2015). Evolution of pollination niches in a generalist plant clade. New Phytologist, 205(1),
440-453.
Couvreur, T. L., Franzke, A., Al-Shehbaz, I. A., Bakker, F. T., Koch, M. A., & Mummenhoff, K.
(2010). Molecular phylogenetics, temporal diversification, and principles of evolution in
the mustard family (Brassicaceae). Molecular Biology and Evolution, 27(1), 55-71.
Salariato, D. L., Manchego, M. A. C., Cano, A., & Al-Shehbaz, I. A. (2019). Phylogenetic
placement of the Peruvian-endemic genus Machaerophorus (Brassicaceae) based on
molecular data and implication for its systematics. Plant Systematics and
Evolution, 305(1), 77-87.
Guo, X., Liu, J., Hao, G., Zhang, L., Mao, K., Wang, X., ... & Koch, M. A. (2017). Plastome
phylogeny and early diversification of Brassicaceae. BMC genomics, 18(1), 176.
Alexander, P. J., Windham, M. D., Govindarajulu, R., Al-Shehbaz, I. A., & Bailey, C. D.
(2010). Molecular phylogenetics and taxonomy of the genus Thysanocarpus
(Brassicaceae). Systematic Botany, 35(3), 559-577.
Huang, C.H., Sun, R., Hu, Y., Zeng, L., Zhang, N., Cai, L., Zhang, Q., Koch, M.A., Al-Shehbaz,
I., Edger, P.P. and Pires, J.C., 2016. Resolution of Brassicaceae phylogeny using nuclear
genes uncovers nested radiations and supports convergent morphological
evolution. Molecular biology and evolution, 33(2), pp.394-412.
Warwick, S. I., Mummenhoff, K., Sauder, C. A., Koch, M. A., & Al-Shehbaz, I. A. (2010).
Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence
data of nuclear ribosomal ITS region. Plant Systematics and Evolution, 285(3-4), 209-232.
Arias, T., Beilstein, M. A., Tang, M., McKain, M. R., & Pires, J. C. (2014). Diversification
times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years
of divergence. American journal of botany, 101(1), 86-91.
Ali, T., Schmuker, A., Runge, F., Solovyeva, I., Nigrelli, L., Paule, J., Buch, A.K., Xia, X., Ploch,
S., Orren, O. and Kummer, V., 2016. Morphology, phylogeny, and taxonomy of
Microthlaspi (Brassicaceae: Coluteocarpeae) and related genera. Taxon, 65(1), 79-98.
Cecchi, L., Gabbrielli, R., Arnetoli, M., Gonnelli, C., Hasko, A., & Selvi, F. (2010).
Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae
(Brassicaceae): evidence from nrDNA sequence data. Annals of Botany, 106(5), 751-767.
Soza, V. L., & Di Stilio, V. S. (2014). Pattern and process in the evolution of the sole
dioecious member of Brassicaceae. EvoDevo, 5(1), 42.
Goodson, B. E., Rehman, S. K., & Jansen, R. K. (2011). Molecular systematics and
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
68
15 NO
NO
Thlaspi
69
70
101 NO
130 NO
NO
NO
71
72
103 NO
56 NO
YES
YES
73
74
223 NO
97 NO
YES
NO
Vella
75
109 NO
NO
Vella
76
49 NO
YES
Pachycladon
77
189 NO
YES
78
195 NO
NO
79
598 NO
YES
80
370 NO
YES
Brassiceae
biogeography of Descurainia (Brassicaceae) based on nuclear ITS and non-coding
chloroplast DNA. Systematic Botany, 36(4), 957-980.
Koch, M., & Al-Shehbaz, I. A. (2004). Taxonomic and phylogenetic evaluation of the
American. Systematic Botany, 29(2), 375-384.
From TreeBase - d13 [R-package APE, Fri May 31 09:08:01 2019]
Salariato, D. L., Manchego, M. A. C., Cano, A., & Al-Shehbaz, I. A. (2019). Phylogenetic
placement of the Peruvian-endemic genus Machaerophorus (Brassicaceae) based on
molecular data and implication for its systematics. Plant Systematics and Evolution,
305(1), 77-87.
From TreeBase - T3061 [R-package APE, Thu Oct 15 18:34:08 2020]
From TreeBase - Parrya [R-package APE, Thu Oct 15 19:34:09 2020] - Nikolov, L.A.,
Shushkov, P., Nevado, B., Gan, X., Al-Shehbaz, I.A., Filatov, D., Bailey, C.D. and Tsiantis, M.,
2019. Resolving the backbone of the Brassicaceae phylogeny for investigating trait
diversity. New Phytologist, 222(3), pp.1638-1651.
From TreeBase - varios [R-package APE, Fri Oct 16 07:38:56 2020]
Simon-Porcar, V. I., Perez-Collazos, E., & Catalan, P. (2015). Phylogeny and systematics of
the western Mediterranean Vella pseudocytisus-V. aspera complex (Brassicaceae). Turkish
Journal of Botany, 39(3), 472-486.
Crespo, M.B., Lledó, M.D., Fay, M.F. and Chase, M.W., 2000. Subtribe Vellinae (Brassiceae,
Brassicaceae): a combined analysis of ITS nrDNA sequences and morphological
data. Annals of Botany, 86(1), pp.53-62.
Joly, S., Heenan, P.B. and Lockhart, P.J., 2009. A Pleistocene inter-tribal
allopolyploidization event precedes the species radiation of Pachycladon (Brassicaceae) in
New Zealand. Molecular phylogenetics and evolution, 51(2), pp.365-372.
German, D.A., Friesen, N., Neuffer, B., Al-Shehbaz, I.A. and Hurka, H., 2009. Contribution
to ITS phylogeny of the Brassicaceae, with special reference to some Asian taxa. Plant
Systematics and Evolution, 283(1-2), pp.33-56.
BrassiBase ITS tree- https://brassibase.cos.uniheidelberg.de/?action=phlv&subaction=Brassiceae
Bailey, C.D., Koch, M.A., Mayer, M., Mummenhoff, K., O'Kane Jr, S.L., Warwick, S.I.,
Windham, M.D. and Al-Shehbaz, I.A., 2006. Toward a global phylogeny of the
Brassicaceae. Molecular biology and evolution, 23(11), pp.2142-2160.
Friesen, N., Čalasan, A.Ž., Neuffer, B., German, D.A., Markov, M. and Hurka, H., 2020.
Evolutionary history of the Eurasian steppe plant Schivereckia podolica (Brassicaceae) and
its close relatives. Flora, p.151602.
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Table S10. List of ecologists kindly sharing unpublished information on Brassicaceae
pollinators. The host institutions are those at the time of the contact with our team.
Last Name
Abdelaziz
Aizen
Aguado
Alarcon
Amat
Arista
Banza
Barbir
Bartomeus
Bergerot
Bommarco
Bosch
Bruinsma
Burkle
CaraDonna
Cartar
Castro
Castro-Urgal
Chacoff
Conner
Cuerda
Dennis
Ebeling
Escudero
Evans
Fernández
Ferrero
Fründ
Fultz
Garbuzov
García
García-Camacho
García
García de Lucas
Giménez
Iriondo
Junker
Kuppler
Lance
Lara
Lázaro
Lorite
Louadi
Loureiro
Lucas-Barbosa
Majetic
Marcos
Medel
Meindl
Melen
Méndez
Menéndez
First Name
Mohamed
Marcelo
Luis Oscar
Ruben
Elena
Montserrat
Paula
Jelena
Ignasi
Benjamin
Riccardo
Jordi
Maaike
Laura
Paul
Ralph
Silvia
Rocio
Natacha
Jeffrey
David
Roger L. H.
Anne
Adrián
Darren
Juande
Victoria
Jochen
Jessica
Mihail
Begoña
Raúl
Yedra
Sandra
Luis
José María
Robert R.
Jonas
Richard
Carlos
Amparo
Juan
Kamel
João
Dani
Cassey J.
Maria Ángeles
Rodrigo
George
Miranda
Marcos
Rosa
Host institution
University of Granada (Spain)
Universidad Nacional del Comahue-CONICET (Argentina)
Castilla y Leon Regional Goverment (Spain)
University Arizona (USA)
Real Jardín Botánico de Madrid (Spain)
University of Seville (Spain)
University of Hull (UK)
ICA-CSIC (Spain)
EBD-CSIC (Spain)
University of Rennes (France)
Swedish University of Agricultural Sciences (Sweden)
CREAF-UAB (Spain)
Leiden University (The Netherlands)
Montana State University (USA)
Northwestern University (USA)
University of Calgary (Canada)
University of Coimbra (Portugal)
IMEDEA-CSIC (Spain)
Universidad Nacional del Comahue-CONICET (Argentina)
Michigan State University (USA)
Junta de Andalucía (Spain)
Staffordshire University (UK)
University of Jena (Germany)
Universidad Rey Juan Carlos (Spain)
University of Hull (UK)
Greenpeace (Spain)
University of León (Spain)
Georg-August-Universität (Germany)
Idaho State University (USA)
University Sussex (UK)
IPE-CSIC (Spain)
Universidad Rey Juan Carlos (Spain)
CIDE (University of New Brunswick)
Junta de Andalucía (Spain)
Universidad Rey Juan Carlos (Spain)
Universidad Rey Juan Carlos (Spain)
University of Salzburg (Austria)
ULM University (Germany)
Northern Arizona University (USA)
Universidad Rey Juan Carlos (Spain)
IMEDEA-CSIC (Spain)
University of Granada (Spain)
University Frères Mentouri Konstantine (Algeria)
University of Coimbra (Portugal)
Wageningen University (The Netherlands)
Saint Mary´s College Indiana (USA)
Universidad de Alicante (Spain)
University of Santiago de Chile (Chile)
Binghamton University (USA)
University of California-Santa Cruz (USA)
Universidad Rey Juan Carlos (Spain)
University of Lancaster (UK)
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Milla
Morales
Morente
Muñoz-Pajares
Norfolk
Norton
O’Malley
Ojeda
Pelayo
Petanidou
Razanajatovo
Roberts
Santamaría
Schlinkert
Schrader
Schupp
Simaika
Simanonok
Stang
Stanley
Stout
Strauss
Torices
Traveset
Tscharntke
Tur
Valido
Valverde
Vargas
Warzecha
Whittall
Winfree
Wonneck
Zink
Rubén
Carolina
Javier
A. Jesus
Olivia
Nicholas
Rachel
Fernando
Roxibel
Theodora
Mialy
S.P.M.
Silvia
Hella
Julian
Eugene W.
John P.
Michael P.
Martina
Dara A.
Jane
Sharon
Rubén
Anna
Teja
Cristina
Alfredo
Javier
Pablo
Daniela
Justen
Rachael
Mark
Lindsay
Universidad Rey Juan Carlos (Spain)
Universidad Nacional del Comahue-CONICET (Argentina)
Universidad Rey Juan Carlos (Spain)
University of Coimbra (Portugal)
University of Nottingham (UK)
Washington State University (USA)
San Jose State University (USA)
University of Cádiz (Spain)
Universidad de las Andes (Venezuela)
University of the Aegean (Greece)
University Konstanz (Germany)
University of Reading (UK)
Universidad Rey Juan Carlos (Spain)
University Goettingen (Germany)
University Goettingen (Germany)
Utah State University (USA)
Stellenbosch University (South Africa)
MSU- Northern Prairie Wildlife Research Center (USA)
University of Leiden (The Netherlands)
Trinity College Dublin (Ireland)
Trinity College Dublin (Ireland)
University of California at Davis (USA)
University Lausanne (Switzerland)
IMEDEA-CSIC (Spain)
University of Göttingen (Germany)
IMEDEA-CSIC (Spain)
IPNA-CSIC (Spain)
EBD-CSIC (Spain)
Real Jardín Botánico de Madrid (Spain)
Goethe University (Germany)
Santa Clara University (USA)
Rutgers University (USA)
University of Calgary (Canada)
University of Calgary (Canada)
Table S11. Brief description of the functional groups of the insects visiting the flowers of the studied species.
Functional Group
Body length
Resource
Behavioural notes
1
Long-tongued extralarge bees
≥ 15 mm
Nectar + Pollen Partially introducing the head in the flower
Legitimate
Hymenoptera
Anthophoridae, Apidae
2
Long-tongued large
bees
10-15 mm
Nectar + Pollen Partially introducing the head in the flower
Legitimate
Hymenoptera
Anthophoridae
3
Long-tongued mediumsized bees
< 10 mm
Nectar + Pollen Partially introducing the head in the flower
Legitimate
Hymenoptera
Anthophoridae
4
Honeybees
6-12 mm
Nectar + Pollen Introducing the whole head in the flower
Legitimate
Hymenoptera
Apidae (Apis spp.)
5
Short-tongued extralarge bees
≥ 15 mm
Nectar + Pollen Introducing the head in the flower
Legitimate
Hymenoptera
Apidae
6
Short-tongued large
bees
> 10 mm
Pollen + Nectar Introducing the whole head in the flower
Legitimate
Hymenoptera
Halictidae, Megachilidae, Colletidae Andrenidae
7
Short-tongued
medium-sized bees
5 – 10 mm
Pollen + Nectar Introducing the whole head in the flower
Legitimate
Hymenoptera
Halictidae, Colletidae, Andrenidae , Apidae
Xylocopinae, Apidae Nomidinae
8
Short-tongued small
bees
2 – 5 mm
Pollen + Nectar They access the nectar legitimately or from between Illegitimate + Hymenoptera
the sepals
Legitimate
Halictidae, Colletidae, Andrenidae , Apidae
Xylocopinae, Apidae Nomidinae
9
Short-tongued extrasmall bees
< 2 mm
Nectar + Pollen They access the nectar legitimately or from between
the sepals
Legitimate + Hymenoptera
Illegitimate
Halictidae, Colletidae
10
Large ants
> 2 mm
Nectar
They can introduce the whole body in the flower to
reach the nectar
Legitimate + Hymenoptera
Illegitimate
Formicidae
11
Small ants
< 2 mm
Nectar
Mostly sipping nectar from between sepals
Illegitimate + Hymenoptera
Legitimate
Formicidae
12
Large pollen wasps
Variable
Pollen
Partially introducing the head in the flower
Legitimate
Hymenoptera
Massarinae
13
Large nectar-collecting
wasps
> 7mm
Nectar
Partially introducing the head in the flower
Legitimate
Hymenoptera
Vespidae
14
Small nectar-collecting
wasps
Usually
< 3mm
Nectar
Mostly sipping nectar from between sepals
15
Hovering long-tongued
Variable
Nectar +
Hovering while nectaring and collecting some pollen
Type of visits Order
Illegitimate + Hymenoptera
Legitimate
Legitimate
Diptera
Examples
Chalcidoidea, Ichneumonoidea
Bombyliidae (Bombylius)
flies
Pollen
16
Non-hovering long
tongued flies
Variable
Nectar
Nectaring without hovering; long buccal apparatus
Legitimate
Diptera
Bombyliidae, Tachinidae, Nemestrinidae,
17
Large hoverflies
>5 mm
Pollen
Collect pollen without entering the flower
Legitimate
Diptera
Syrphidae (Eristalini)
18
Small hoverflies
< 5 mm
Pollen +
Nectar
Collect pollen without entering the flower and
sometimes sip nectar from between the sepals
Legitimate + Diptera
Illegitimate
Syrphidae
19
Large flies
>5 mm
Nectar +
Pollen
Collect pollen without entering the flower and
nectar
Legitimate + Diptera
Illegitimate
Muscidae, Calliphoridae, Tabanidae,
Scatophagidae, Anthomyiidae
20
Small flies
< 5 mm
Nectar +
Pollen
Mostly sipping nectar
Illegitimate + Diptera
Legitimate
Muscidae, Anthomyiidae, Micetophyliidae,
Drosophilidae, Stratiomyidae
21
Long tongued small
flies
< 5 mm
Nectar
Sipping nectar
Illegitimate + Diptera
Legitimate
Bibionidae, Empididae
22
Large beetles
> 7 mm
Mostly Pollen
Consuming not only pollen, also anthers, petals, and
other floral parts
Legitimate + Coleoptera
Illegitimate
Cetonidae, Lagridae, Mylabridae, Allecuninae
23
Small beetles
< 7 mm
Pollen + Nectar Consuming pollen during legitimate visits and also
robbing nectar from the bottom part of the flowers
Legitimate + Coleoptera
Illegitimate
Melyridae (Malachidae, Dasytidae), Cleridae,
Oedemeridae, Elateridae, Bruchidae, Buprestidae,
Chrysomelidae
24
Small diving beetles
<3 mm
Nectar + Pollen Entering completely into the flower, crawling down
the corolla for nectar
25
Large Butterflies
≥ 20 mm
Nectar
26
Small Butterflies
< 20 mm
27
Hawkmoths
28
Legitimate
Coleoptera
Nitidulidae, Dermestidae, Phalacridae
Feeding on nectar both from inside the flower and
between the sepals
Legitimate
Lepidoptera
Nymphalidae, ,Papilionidae, Pieridae
Nectar
Feeding on nectar both from inside the flower and
between the sepals
Legitimate
Lepidoptera
Lycaenidae, Pieridae, Hesperidae
> 7 mm
Nectar
Hovering to sip nectar
Legitimate
Lepidoptera
Sphingidae
Large moths
> 3mm
Nectar
Sipping nectar while landed onto the corolla
Legitimate
Lepidoptera
Crambidae, Noctuidae
29
Small moths
< 3mm
Nectar
Sipping nectar without entering the flower
30
Nocturnal moths
variable
Nectar
Sipping nectar while landed onto the corolla or by
hovering; Visiting the flowers at night
Illegitimate + Lepidoptera
Legitimate
Legitimate
Lepidoptera
Adelidae, Plutellidae
Noctuidae
31
Bugs
variable
Nectar
Sipping nectar without entering the flower. Also
acting as sapsuckers in vegetative tissues
Legitimate + Hemiptera
Illegitimate
32
Thrips
< 3 mm
Pollen
Feeding from inside the flowers
Legitimate
Thysanoptera
33
Grasshoppers
variable
Pollen + Floral
parts
Mostly nymphs
Legitimate
Orthoptera
34
Aphids
< 2 mm
Nectar
Mostly winged individuals
Legitimate
Hemiptera
35
Earwig
> 15 mm
Pollen
Legitimate + Dermaptera
Illegitimate
36
Lacewing
> 15 mm
Pollen + Nectar
Legitimate + Neuroptera
Illegitimate
37
Snakeflies
> 8 mm
Pollen + Nectar
Legitimate + Raphidioptera
Illegitimate
38
Birds
>>> 15 mm
Nectar
Legitimate
39
Springtails
< 2 mm
Nectar
Legitimate +
Illegitimate
40
Mites
< 2 mm
Nectar
Legitimate +
Illegitimate
41
Spiders
< 2 mm
Unknown
Illegitimate
42
Larvae
variable
Unknown
Illegitimate
43
Others
variable
Unknown
Illegitimate
Passeriformes
Lygaeidae, Pentatomidae
Aphidoidea
Chrysopidae
bioRxiv preprint doi: https://doi.org/10.1101/2021.05.25.445642; this version posted May 26, 2021. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.
Francisco Perfectti