|
Received: 25 July 2018
Revised: 24 January 2019
|
Accepted: 25 January 2019
DOI: 10.1002/ece3.4987
ORIGINAL RESEARCH
Biogeography of the xerophytic genus Anabasis L.
(Chenopodiaceae)
Maximilian Lauterbach1,2,3
4
P. Sukhorukov
| Marie Claire Veranso‐Libalah1,2
| Alexander
1,2
| Gudrun Kadereit
1
Institut für Molekulare
Physiologie, Johannes Gutenberg‐
Universität Mainz, Mainz, Germany
Institut für Organismische und Molekulare
Evolutionsbiologie, Johannes Gutenberg‐
Universität Mainz, Mainz, Germany
2
School of Molecular Sciences, University of
Western Australia, Perth, WA, Australia
3
Department of Higher Plants, Biological
Faculty, Moscow Lomonosov State
University, Moscow, Russia
4
Correspondence
Maximilian Lauterbach, School of Molecular
Sciences, University of Western Australia,
Perth, WA, Australia.
Email: max.lauterbach@uwa.edu.au
Funding information
GEOCYCLES; Russian Fond for Basic
Research, Grant/Award Number:
18‐04‐00029
Abstract
Aim: Using the extremophile genus Anabasis, which includes c. 28 succulent, xero‐
phytic C4 species, and is widely distributed in arid regions of Northern Africa, Arabia,
and Asia, we investigate biogeographical relationships between the Irano‐Turanian
floristic region (ITfr) and its neighboring regions. We test whether the spread of arid
and semi‐arid biomes in Eurasia coincides with the biogeography of this drought‐
adapted genus, and whether the ITfr acted as source area of floristic elements for
adjacent regions.
Location: Deserts and semi‐deserts of Northern Africa, Mediterranean, Arabia, West
and Central Asia.
Methods: Four cpDNA markers (rpL16 intron, atpB‐rbcL, trnQ‐rps16, and ndhF‐rpL32
spacers) were sequenced for 58 accessions representing 21 Anabasis species.
Phylogenetic relationships and divergence times were inferred using maximum likeli‐
hood and a time‐calibrated Bayesian approach. To document the extant distribution
of Anabasis, material from 23 herbaria was surveyed resulting in 441 well‐docu‐
mented collections used for the coding of eight floristic regions. Using this coded
data, ancestral range was estimated using “BioGeoBEARS” under the DEC model.
Results: Anabasis originated during the Late Miocene and the ancestral range was
probably widespread and disjunct between Western Mediterranean and the Irano‐
Turanian regions. Diversification started with two divergence events at the Miocene/
Pliocene boundary (5.1 and 4.5 mya) leading to Asian clade I with ITfr origin which is
sister to a slightly younger Asian clade II, which originated in the Western ITfr, and a
Mediterranean/North African clade with an origin in the Western Mediterranean.
Main conclusions: Anabasis did not follow aridification and continuously expanded
its distribution area, in fact its probably wide ancestral distribution area seems to
have been fragmented during the very Late Miocene and the remnant lineages then
expanded into neighboring arid regions. This genus supports the role of the ITfr as
source area for xerophytic elements in the Mediterranean and Central Asia.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Ecology and Evolution. 2019;1–14.
www.ecolevol.org
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LAUTERBACH ET AL.
KEYWORDS
ancestral range estimation, arid and semi‐arid deserts, Eurasian deserts, Irano‐Turanian
floristic region, mediterranean region, molecular phylogeny, succulence, xerophyte
1 | I NTRO D U C TI O N
been proposed (Takhtajan, 1986; Zohary, 1973). Consequently,
some authors hypothesized that the ITfr served as a source area
The Irano‐Turanian floristic region (ITfr) as defined by Griesebach
for the adjacent floristic regions (Comes, 2004; Djamali et al., 2012;
(1884) and Takhtajan (1986) covers c. 30% of Eurasia and ranges
Manafzadeh, Salvo, & Conti, 2014; Manafzadeh et al., 2017; Roquet
from southern parts of Mongolia and western provinces of China,
et al., 2009; Zhang et al., 2014; Zohary, 1973), mostly because a sta‐
Kyrgyzstan, Tajikistan, Pakistan, Afghanistan, southern parts of
ble dry climate has persisted in some parts of the ITfr since the early
European Russia, Kazakhstan, Uzbekistan, Turkmenistan, Iran, and
Eocene, hence providing a stable habitat for plant lineages over a long
Iraq to the Anatolian plateau, inland parts of Syria and Lebanon,
time (Manafzadeh et al., 2014, 2017). Studies in Apiaceae (Banasiak
and Jordan. The ITfr harbors more than 27,000 species in its spe‐
et al., 2013), Brassicaceae (Franzke, Lysak, Al‐Shehbaz, Koch, &
cies‐rich western part and around 5,000 species in its eastern part
Mummenhoff, 2011; Karl & Koch, 2013), and Rutaceae (Manafzadeh
(Manafzadeh, Staedler, & Conti, 2017 and ref. therein). The degree
et al., 2014) support this hypothesis. However, only few molecular,
of endemism in the ITfr ranges between 20%–40% (Takhtajan,
historical biogeographic studies have so far been conducted that rig‐
1986; Zohary, 1981) and is particularly high in the three biodiver‐
orously tested relationships between the ITfr and recipient areas as
sity hotspots of the western ITfr: the Irano‐Anatolian region, the
well as possible dispersal events or migration routes. In particular,
Mountains of Central Asia, and the Caucasus (see Manafzadeh et al.,
the biogeographical study of the xerophytic Haplophyllum A. Juss.
2017; Solomon, Shulkina, & Schatz, 2013). Among a number of fea‐
(Rutaceae) supported the role of the western ITfr as a source area
tures described as characteristic for the ITfr is the high diversity of
for xerophytic elements found in the Mediterranean (Manafzadeh
Chenopodiaceae (sensu Walker et al., 2018), especially in desert
et al., 2014). Though, additional studies of the ITfr plant lineages are
and semi‐desert areas (summarized in Djamali, Brewer, Breckle, &
needed to test a putatively source‐like character of the ITfr using
Jackson, 2012; Manafzadeh et al., 2017). In these arid areas, the
biogeographical analyses of dated phylogenies in order to put diver‐
vegetation is dominated by a high number of C4 chenopods species
gence and diversification into time and space.
(Manafzadeh et al., 2017; Schüssler et al., 2017; Takhtajan, 1986). C4
As a monophyletic lineage within the ITfr typical element
photosynthesis is a recently evolved elaboration of the conventional
Salsoleae‐Chenopodiaceae, with a proposed stem age dating back to
photosynthetic carbon reduction cycle, also known as C3 pathway,
the Miocene (Schüssler et al., 2017), the xerophytic genus Anabasis
to concentrate CO2 for utilization by ribulose‐1,5‐bisphosphate car‐
L. is suitable to investigate the relationships of xerophytic elements
boxylase/oxygenase (RuBisCO) in the Calvin cycle (Hatch, 1987).
of the ITfr and its adjacent regions. According to literature and flora
Only c. 3% of the angiosperms conduct C4 photosynthesis, and with
treatments, Anabasis is widely distributed in steppes, semi‐deserts
more than 750 C4 species, the family Chenopodiaceae comprises the
largest number of C4 species in the eudicots (Kadereit, Ackerly, &
Pirie, 2012; Sage, Christin, & Edwards, 2011).
and deserts of North Africa, West and Central Asia (Hedge, 1997;
Sukhorukov, 2008), and it also occurs in the most southern parts of
Spain, the Eastern Mediterranean, South Siberia, West China, and
Aridification in the ITfr started during the Eocene–Oligocene
Mongolia. Hence, with this wide distribution Anabasis covers not
transition and intensified during the Middle Miocene–Pliocene
only the entire ITfr but is also present in most adjacent floristic re‐
(Zhang et al., 2014). In this latter phase, uplifts of mountain chains
gions, thus a perfect candidate genus to infer the floristic relation‐
and plateaus (e.g., Alborz, Tien Shan, Zagros) caused large rain shad‐
ships among these areas and eventually to test whether the ITfr acts
ows, continuous temperature decrease, and increased continentality,
as source area for adjacent regions.
which likely triggered the expansion of xerophytic plant communi‐
Anabasis belongs to subfamily Salsoloideae (tribe Salsoleae), one
ties in the ITfr (Manafzadeh et al., 2017 and ref. therein). According
of the oldest C4 clades in Chenopodiaceae (Kadereit et al., 2012;
to Djamali et al. (2012), the three climatic factors, continentality,
Schüssler et al., 2017), and comprises c. 28 species (Hedge, 1997;
winter temperature, and precipitation seasonality, differentiate the
Sukhorukov, 2008). Except for A. annua Bunge, which is a thero‐
ITfr from its adjacent territories, the Mediterranean, the Saharo‐
phyte, the remaining species of Anabasis (including the former genera
Arabian, Euro‐Siberian and the Central Asiatic regions. Among these
Brachylepis C.A. Mey., Fredolia Coss. & Durieu and Esfandiaria Charif
three factors, continentality was found to be the prime factor that
& Aellen; Hedge, 1997) are nanophanerophytes and chamaephytes
separates the ITfr from Mediterranean and Saharo‐Arabian regions
often with a thick and woody caudex (Figure 1). The typical morpho‐
and also the main factor separating sub‐regions within the ITfr itself
logical characters of the genus are fleshy annual shoots, usually with
(Djamali et al., 2012).
reduced or very short subulate opposite leaves and numerous tri‐
Based on floristic similarities, a close relationship of the ITfr
chomes at the leaf bases (Figure 1; Hedge, 1997; Sukhorukov, 2008).
to the Mediterranean region and Saharo‐Arabian region has long
Many species of Anabasis are able to grow in extremely dry and
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LAUTERBACH ET AL.
(a)
(b)
3
(c)
(d)
F I G U R E 1 Representative specimens
of Anabasis showing typical growth
forms of the genus. Several species
are nanophanerophytes with a highly
compact growth form with a deep, woody
taproot, and a cushion‐like aboveground
appearance (b, c, d), while others show a
more open and spreading growth of the
shoots (chamaephytes; a, e, f, g), A. annua
(h) is the only therophyte in the genus.
Leaves are mostly short or completely
reduced, and photosynthesis is taken
over by the green shoots. a. A. salsa (coll.
I.O. Baitulin et al. s.n. (28.06.1997, K),
Kazakhstan), b. A. calcarea (coll. K.H.
Rechinger 50209 (B), Iran), c. A. articulata
(coll. Danin et al. 26058 (B), Israel), d.
A. aretioides (coll. I. Breitwieser & R.W.
Vogt 385 (B), Morocco), and e. A. eugeniae
(coll. J. Lamond 3896 (E), North Iran)
have the largest leaves in the genus,
f. A. brevifolia (coll. W. Hilbig et al. s.n.
(04.07.1978; HAL), Mongolia), g. A. syriaca
(coll. J. E. Clarke & A.M. Clarke 13 (E),
Jordan), and h. A. annua (coll. Assadi &
Abouhamzeh 36523 (TARI), Iran). Scale
bars: a‐c and e‐h = 5 cm, d = 2 cm
(f)
(e)
(g)
(h)
harsh environments surpassing the stress tolerance of most other
markers, its biogeographic origin and expansion in the ITfr adjacent
plant species and thereby in some extremely hostile areas forming
regions were reconstructed to test whether the ITfr served as a
characteristic species‐poor vegetation types (Bokhari & Wendelbo,
source of species to the recipient regions, and whether Anabasis fol‐
1978; Kürschner, 2004). While most species of Anabasis seem to be
lowed the spread of arid biomes in Eurasia and North Africa.
restricted in their distribution, others for example, A. aphylla and
A. salsa (both from Eastern Europe and Asia Minor to Central Asia)
and A. setifera Moq. (in the Saharo‐Arabian province) are known to
be more widespread (Flora of China at http://www.efloras.org; Flora
of Pakistan at http://www.tropicos.org; Hedge, 1997; Maire, 1962).
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Phylogenetic inference and molecular dating
However, the current assessment of the distribution of Anabasis spe‐
DNA was extracted from 58 accessions representing 21 species of
cies is relatively rough and likely incomplete.
Anabasis. A broad outgroup of Salsoloideae and Camphorosmoideae
Here, we conducted a survey of c. 600 available herbarium speci‐
was included according to Schüssler et al. (2017; see Supporting
mens of 28 species of Anabasis to infer their distribution areas. Using
Information Appendix S1). The samples for phylogenetic analyses
a resolved and dated molecular phylogeny based on 58 accessions
were carefully chosen for a better representation of the entire
representing 21 species of Anabasis and data from four chloroplast
distributional range of Anabasis. Samples were taken mainly from
4
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LAUTERBACH ET AL.
well‐preserved herbarium specimens or from recently collected
2014). Outgroup (Suaedoideae and Salicornioideae) as well as the
and silica‐dried material. Representatives of Suaedoideae (Suaeda
ingroup (all others) was treated as monophyletic and the age of
altissima Pall. and S. aralocaspica (Bunge) Freitag & Schütze) and
the most recent common ancestor (tmrca) for the ingroup was
Salicornioideae (Allenrolfea occidentalis Kuntze, Arthrocaulon mac‐
calibrated using a normal distribution prior with a mean of 30.75
rostachyum (Moric.) Piirainen & G.Kadereit, Halopeplis perfoliata
and sigma of 5.55, matching the 95% highest posterior density
Bunge ex Schweinf. & Asch., Kalidium cuspidatum (Ung.‐Sternb.)
(HPD; 39.9–21.6 mya) of Kadereit, Newton, and Vandelook (2017).
Grubov and Tecticornia triandra (F. Muell.) K.A.Sheph. & Paul
For the BEAST analysis, we used the substitution model GTR+γ
G.Wilson) served as outgroup for the phylogenetic analyses (see
with four gamma categories. The uncorrelated lognormal relaxed
Supporting Information Appendix S1). DNA isolation, PCR, and
clock under a Birth–Death speciation process (Gernhard, 2008;
sequencing of the four cpDNA markers, rpl16 intron, atpB‐rbcL,
Nee, May, & Harvey, 1994) with a random starting tree was set
ndhF‐rpL32, and trnQ‐rps16 spacers, followed the same proce‐
for the molecular dating analysis. The Markov chain Monte Carlo
dures as outlined in Schüssler et al. (2017). Chromatograms result‐
(MCMC) ran for 50 million generations and sampling every 5,000
ing from Sanger‐sequencing on an automatic sequencing machine
generations. The performance of the BEAST run was checked in
of type 3130XL (Applied Biosystems™) were edited and aligned
TRACER v.1.6 (Rambaut, Suchard, & Drummond, 2014) using the
using Mega v.5 (Tamura et al., 2011).
BEAST log file. The first 10 percent of the sampled trees were dis‐
To find the best substitution model for the maximum likelihood (ML)
carded as “burn‐in.” The remaining trees were summarized using
and Bayesian calculations, we used the JMODELTEST v.2.1.4 (Darriba,
TREEANNOTATOR v.2.4.5 (Bouckaert et al., 2014), and 95% con‐
Taboada, Doallo, & Posada, 2012) on CIPRES Science Gateway v.3.3
fidence limits for ages of the nodes were calculated.
(Miller, Pfeiffer, & Schwartz, 2010). Based on the Akaike information
criterion (AIC), the best fitting model was the GTR+γ model. The ML
2.2 | Biogeographic analyses and species
distribution
analyses were carried out using RAxML v.8 (Stamatakis, 2014).
Calibration of the molecular clock and calculation of divergence
times were performed using BEAST v.2.4.5 (Bouckaert et al., 2014)
The assessment of the distribution of the species was based on a
on CIPRES Science Gateway v.3.3 (Miller et al., 2010). The BEAST
survey of c. 600 herbarium specimens which were loaned from B,
xml input files were created with BEAUti v.2.4.5 (Bouckaert et al.,
BCN, BEI, BM, E, GLM, HAL, K, KAS, LE, M, MJG, MO, MPU, MSB,
g
h
e
a
f
b
d
c
F I G U R E 2 Distribution area of Anabasis as inferred from 441 georeferenced specimens. Anabasis is distributed in eight geographic
areas based on the floristic regions of the world (Takhtajan, 1986): (a) Southern Moroccan Province, Southwestern Mediterranean Province,
South Mediterranean Province; (b) Saharan Province; (c) Northern part of Sudano‐Zambezian Region; (d) Egyptian‐Arabian Province; (e)
Mesopotamian Province, Armeno‐Iranian Province, Hyrcanian Province; (f) Turkestanian Province, Northern Baluchistanian Province,
Western Himalayan Province; (g) Turanian or Aralo‐Caspian Province, Dzhungaro‐Tien Shan Province; and (h) Mongolian Province (see also
Table 1)
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LAUTERBACH ET AL.
5
TA B L E 1 Sampling of Anabasis species in the phylogenetic and biogeographical analyses and number of specimens included in the
assessment of distribution area for each species
Species of Anabasis (28 spp. in
total)
Samples in molecular phylogenetic analysis
(corresponding to Chen No. in Supporting
Information Appendix S1); samples used in
the biogeographical analysis in bold
No of specimens included in
the assessment of distribution
area (Supporting Information
Appendix S2)
Coding for biogeo‐
graphical analyses
A. annua Bunge
1837, 1838
9
EG
A. aphylla L.
1836, 2017, 2358, 2743
27
EG
A. aff. aphylla (distributed in
Mongolia)
2411
9
H
A. aretioides Moq. & Coss. ex Bunge
0087, 2424, 2544, 2545
17
AB
A. articulata (Forssk.) Moq.
2359, 2360, 2379
39
BD
A. brachiata Kar. & Kir.
Not sampled
6
(EG)
A. brevifolia C.A.Mey.
2361, 2406, 2407, 2416
21
H
A. calcarea (Charif & Aellen) Bokhari
& Wendelbo
1841, 1852, 2363
13
E
A. cretacea Pall.
2011
16
G
A. ebracteolata Korov. ex Botsch.
2013, 2538
5
G
A. ehrenbergii Schweinf. ex Boiss.
2403, 2741
11
(C)
A. elatior (C.A.Mey.) Schischk.
2541, 2542
7
GH
A. eriopoda (Schrenk) Benth. ex
Volkens
2434, 2531, 2532
15
EG
A. eugeniae Iljin
1843, 1844
5
E
A. ferganica Drobov
Not sampled
1
(G)
A. haussknechtii Bunge ex Boiss.
1842, 1845, 1847, 1848
12
EF
A. aff. jaxartica (distributed in
Persia)
1849, 2384
4
E
A. jaxartica (Bunge) Benth. ex Iljin
(distributed in Central Asia)
2540
3
G
A. lachnantha Aellen & Rech.f.
1834, 2547
18
CD
A. macroptera Moq.
Not sampled
8
(F)
A. oropediorum Maire
1767, 2745
34
AB
A. aff. oropediorum (distributed in
Morocco)
2370
1
A
A. pelliotii Danguy
Not sampled
1
(G)
A. prostrata Pomel
1227, 1471
12
A
A. salsa (C.A.Mey.) Benth. ex
Volkens
2019, 2539
18
EG
A. aff. salsa (distributed in Mongolia)
2413
2
H
A. setifera Moq.
2012, 2372, 2373
80
CDEF
A. syriaca Iljin
1468, 2421, 2418
26
ADE
A. tianschanica Botsch.
Not sampled
1
(G)
A. truncata (Schrenk) Bunge
2408, 2409
10
GH
A. turgaica Iljin & Krasch.
Not sampled
1
(G)
A. turkestanica Korovin & Iljin
Not sampled
9
(FG)
Total
∑ 58 (24 in biogeo. analysis representing 21
currently recognized species)
∑ 441
For full voucher information, see Supporting Information Appendix S2 in the online supplement. Coding of biogeographical areas: A = Southern
Moroccan Province, Southwestern Mediterranean Province, South Mediterranean Province; B = Saharan Province; C = Northern part of Sudano‐
Zambezian Region; D = Egyptian‐Arabian Province; E = Mesopotamian Province, Armeno‐Iranian Province, Hyrcanian Province; F = Turkestanian
Province, Northern Baluchistanian Province, Western Himalayan Province; G = Turanian or Aralo‐Caspian Province, Dzhungaro‐Tien Shan Province;
and H = Mongolian Province.
6
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LAUTERBACH ET AL.
MW, STU, TARI, TUH, UPS, W, and WU. A total of 441 confidently
bp and includes 58 accessions of Anabasis representing 21 species.
identified specimens were selected and georeferenced (Supporting
The ML analysis (not shown) and the Bayesian analysis (see Supporting
Information Appendix S2). A distribution map for each species and
Information Appendix S4) revealed identical topologies. Anabasis (excl.
for the genus as a whole was generated using QGIS v.2.14 (QGIS
A. ehrenbergii Schweinf. ex Boiss.) is monophyletic with high support.
Developmental TEAM, 2009; Figure 2, Supporting Information
Anabasis ehrenbergii is solved as sister to the remaining Anabasis spe‐
Appendix S3). Eight geographic areas based on the floristic regions
cies, albeit with only low support (posterior probability 0.94). In previ‐
of the world (Takhtajan, 1986) and the extant distribution of Anabasis
ous studies with less accessions of Anabasis, A. ehrenbergii was in an
derived from the georeferenced herbarium material were coded:
unresolved position among other members of the Salsoleae (Schüssler
A = Southern Moroccan Province, Southwestern Mediterranean
et al., 2017). The position of Anabasis within Salsoleae still remains
Province, South Mediterranean Province; B = Saharan Province;
poorly resolved (as in Schüssler et al., 2017). For all species except
C = Northern part of Sudano‐Zambezian Region; D = Egyptian‐
A. cretacea Pall., multiple accessions from different regions were in‐
Arabian Province; E = Mesopotamian Province, Armeno‐Iranian
cluded and all but four species are resolved as monophyletic (Figure 3).
Province, Hyrcanian Province; F = Turkestanian Province, Northern
The four species that are probably not monophyletic are A. aphylla L.,
Baluchistanian Province, Western Himalayan Province; G = Turanian
A. jaxartica (Bunge) Benth. ex Iljin, A. oropediorum Maire, and A. salsa
or Aralo‐Caspian Province, Dzhungaro‐Tien Shan Province; and
(C.A.Mey.) Bentham ex Volkens. For A. aphylla, A. oropediorum, and
H = Mongolian Province (see Table 1; Figure 2). The ITfr is repre‐
A. salsa, we found evidence that accessions from strongly disjunct
sented by the regions D, E, F, G, and southernmost part of H.
areas of their species distribution (accessions from Morocco in case
For the biogeographical analyses, another BEAST analysis was
of A. oropediorum and accessions from Mongolia in case of A. aphylla
performed using nearly the same settings as above but with a re‐
and A. salsa) formed separate clades (Figure 3, Supporting Information
duced data set that included only one accession per species to avoid
Appendix S4). This might indicate that these species are currently not
any errors due to sampling bias, that is multiple accessions of some
well‐defined. In these three cases, we separated the disjunct areas for
species versus only one accession in other species. For monophy‐
the subsequent biogeographical analysis.
letic species, the accession with the most sequence information
Anabasis (excl. A. ehrenbergii) shows three major clades (marked
available was included in the analysis, while for the four polyphy‐
in Figures 3,4, Supporting Information Appendix S4): CLADE 1
letic species two accessions per species were used for the analysis
(the Asian clade I in Figures 3,4) comprises A. truncata, A. brevifo‐
(see Table 1; Results section). The calibration derived from the first
lia, A. cretacea, A. setifera, A. annua, A. lachnantha, and A. eugeniae.
BEAST analysis for the crown node of Anabasis (excl. A. ehrenbergii)
Anabasis annua is probably nested within A. setifera; CLADE 2 (the
was used (normal prior with mean of 5.21 and sigma of 1.79, 95%
Asian clade II in Figures 3,4) comprises A. hausknechtii, A. ebracteo‐
HPD: 8.14–2.26 mya), and a MCMC of 25 million generations sam‐
lata, A. syriaca, A. aphylla, A. salsa, A. elatior, A. jaxartica, A. calcarea,
pling every 2500 generations. Ancestral range estimation (ARE) was
A. eriopoda, A. aff. jaxartica as well as A. aff. aphylla and A. aff. salsa
conducted using “BioGeoBEARS” (Matzke, 2013, 2014) in R v.3.3.2
from Mongolia; CLADE 3 (the Mediterranean/North African clade in
(R Core Team, 2016). Due to recent criticism of the dispersal–ex‐
Figures 3,4) comprises A. aretioides, A. prostrata. A. articulata, A. oro‐
tinction–cladogenesis, DEC+J model of founder‐event speciation
pediorum, and A. aff. oropediorum from Morocco with accessions of
model (Ree & Sanmartín, 2018), we excluded all +j models and only
A. articulata and A. oropediorum in a polytomy.
conducted the biogeographic analyses under a dispersal–extinc‐
The crown age of Anabasis including A. ehrenbergii (or stem age
tion–cladogenesis model (DEC model), dispersal–vicariance model
of Anabasis excl. A. ehrenbergii) dates back to 6.88 mya (95% HPD:
(DIVALIKE model), and BAYAREA model (BAYAREA model). The
12.1–3.5 mya) which suggests that the genus originated during the
maximum credibility tree generated from the second BEAST anal‐
Late Miocene. The age estimate of the stem of Anabasis including
ysis (representing one accession per species, see above) was used
A. ehrenbergii is inaccurate due to the poor resolution in this part of
as input to the ARE. We allowed the inferred ancestor to occupy a
the tree. However, it is probably not older than 9.2 mya (95% HPD:
maximum of four areas, corresponding to the maximum number of
14.4–4.3 mya) which is the crown age of the next deeper highly sup‐
areas occupied by any extant species.
ported node in the tree (Supporting Information Appendix S4). The
three major clades originated at the Miocene/Pliocene boundary
3 | R E S U LT S
(5.1–4.5 mya; Figure 3, Supporting Information Appendix S4).
3.1 | Molecular phylogeny and dating
3.2 | Biogeographical analyses
The combined dataset of all four chloroplast markers (rpl16 intron,
Based on the likelihood and AIC values, the best fit model was the
atpB‐rbcL, trnQ‐rps16, and ndhF‐rpL32 spacers) comprises 4546 aligned
DEC model (Table 2). No clear ancestral area could be estimated for
F I G U R E 3 Time‐calibrated tree generated in BEAST2 of 58 accessions representing 21 species of Anabasis. Posterior probabilities
resulting from the Bayesian analysis above branches. Accessions marked by an asterisk indicate the potential polyphyly of those species.
This is a cutout of the full time‐calibrated tree of Salsoleae shown in Supporting Information Appendix S4 in the online supplement
|
LAUTERBACH ET AL.
0.78
0.82
1
1.5
2.17
1
1
1
1
1.51
0.14
1 1.06
3.17
1
0.76
0.99
1.06
0.46
1
1
1
4.53
1.77
2.79
1
0.68
1.41
1 1
0.99
1
0.78
2.02
1
0.17
1
0.78
1
1
3.69
1
0.37
1
5.07
1
1.14
0.26
1
0.99
0.97
0.98
0.46
2.19 1.54
2.86
1
1 0.33
2.45
0.94
0.15
0.69 1
0.97
1
1.18
6.88
4.5
0.94
1 0.15
0.95
2.16
1
2.91
1
0.99
0.63
3.81
1
0.21
1
1.79
10.0
5.0
0.0
Anabasis aretioides 0087
Anabasis aretioides 2424
Anabasis aretioides 2545
Anabasis aretioides 2544
Anabasis aff. oropediorum 2370 *
Anabasis oropediorum 1767
Anabasis oropediorum 2745
Anabasis articulata 2360
Anabasis articulata 2359
Anabasis articulata 2379
Anabasis prostrata 1227
Anabasis prostrata 1471
Anabasis syriaca ssp. africana 1468
Anabasis syriaca ssp. africana 2421
Anabasis syriaca ssp. africana 2418
Anabasis ebracteolata 2013
Anabasis ebracteolata 2538
Anabasis haussknechtii 1842
Anabasis haussknechtii 1847
Anabasis haussknechtii 1848
Anabasis haussknechtii 1845
Anabasis aphylla 1836
Anabasis aphylla 2743
Anabasis aphylla 2017
Anabasis aphylla 2358
Anabasis salsa 2019
Anabasis salsa 2539
Anabasis elatior 2541
Anabasis elatior 2542
Anabasis aff. aphylla 2411*
Anabasis aff. salsa 2413 *
Anabasis aff. jaxartica 1849 *
Anabasis aff. jaxartica 2384 *
Anabasis calcarea 1841
Anabasis calcarea 1852
Anabasis calcarea 2363
Anabasis eriopoda 2434
Anabasis eriopoda 2531
Anabasis eriopoda 2532
Anabasis jaxartica 2540
Anabasis lachnantha 1834
Anabasis lachnantha 2547
Anabasis eugeniae 1843
Anabasis eugeniae 1844
Anabasis annua 1837
Anabasis annua 1838
Anabasis setifera 2012
Anabasis setifera 2373
Anabasis setifera 2372
Anabasis cretacea 2011
Anabasis brevifolia 2361
Anabasis brevifolia 2406
Anabasis brevifolia 2407
Anabasis brevifolia 2416
Anabasis truncata 2408
Anabasis truncata 2409
Anabasis ehrenbergii 2403
Anabasis ehrenbergii 2741
CLADE 3 =
Mediterranean/
North African
clade
CLADE 2 =
Asian clade II
CLADE 1 =
Asian clade I
Anabasis
ehrenbergii
7
8
|
LAUTERBACH ET AL.
TA B L E 2
Results of the biogeographical analysis using BioGeoBEARS
Model
LnL
No. of param.
d
e
j
AIC
AIC wt
AICc
AICc wt
BAYAREALIKE
−90.19
2
0.03
0.28
0
189.3
0.73
184.9
0.082
DIVALIKE
−89.98
2
0.043
1.0e‐12
0
185.6
0.64
184.5
0.1
DEC
−89.57
2
0.035
1.0e‐12
0
186.3
0.38
183.7
0.15
the crown node of Anabasis (excl. A. ehrenbergii; Figure 4), and only
2013) or tribe Cardueae, Compositae (Barres et al., 2013). Also,
three widespread and disjunct ancestral distribution areas got p values
Jabbour and Renner (2011) could show strong biogeographical links
≥0.05 (AEGH: p = 0.08, AE: p = 0.06, AEH: p = 0.05; Figure 4). These
between the ITfr and the Mediterranean region in tribe Delphinieae
area combinations are not restricted to areas belonging to the ITfr, but
(Ranunculaceae). Furthermore, even if not the geographical origin,
also include the Southern Moroccan/Southwestern Mediterranean/
the ITfr was proposed to be a major center of diversification in sub‐
South Mediterranean Provinces (A) and the Mongolian Province (H).
family Apioideae, Apiaceae (Banasiak et al., 2013) or the Campanula
The ancestral range of the crown of the Asian clade I (CLADE 1) clearly
alliance, Campanulaceae (Roquet et al., 2009). Besides these ex‐
excludes western parts of the genus distribution area and was either
amples of plant groups inhabiting rather temperate habitats, the
located in the Mesopotamian Province/Armeno‐Iranian/Hyrcanian (E:
ITfr was suspected as the likely source area especially for arid taxa
p = 0.14) or in E combined with the Mongolian Province (EH: p = 0.07)
found in neighboring regions, in particular in the Mediterranean area
or the Turanian and Aralo‐Caspian Province, Dzhungaro‐Tien Shan
(Blondel, Aronson, Bodiou, & Boeuf, 2010; Comes, 2004; Quézel,
Province (EG: p = 0.05) (Figure 4). All these three areas represent a
1985; Takhtajan, 1986; Zohary, 1973). Arid regions play an essential
possible origin in the ITfr for the Asian clade I.
role for terrestrial biomes, as the desert and semi‐desert biomes oc‐
The ancestral distribution area, for the node from which the Asian
cupy together more than one‐third of the global land surface (Laity,
clade II and Mediterranean clade (CLADES 2 and 3, respectively) are de‐
2008). Within the desert and semi‐desert biomes, the combined
rived, was clearly inferred as disjunct between the Southern Moroccan/
hyperarid, arid, and semi‐arid regions of North Africa and Eurasia
Southwestern Mediterranean/South Mediterranean Provinces and the
are larger than all remaining dry areas of the world. The enormous
Mesopotamian/Armeno‐Iranian/Hyrcanian provinces (AE: p = 0.35),
deserts and steppes of North Africa and Eurasia reach in a contin‐
albeit three further areas received p values ≥0.05 distribution area
uous, broad belt from the Atlantic coast of North Africa, through
(Figure 4). The crown nodes of the Asian clade II were reconstructed
the Arabian Peninsula into southern and Central Asia, including the
as the Mesopotamian Province/Armeno‐Iranian/Hyrcanian (E: p = 0.32;
Sahara, the Arabian Desert, the Syrian Desert, Dasht‐e Lut, Dasht‐e
Figure 4) while that of the Mediterranean/North African clade was re‐
Kavir, Karakum, Taklamakan, and Gobi (Laity, 2008). However, bio‐
constructed as the Southern Moroccan/Southwestern Mediterranean/
geographical studies specifically investigating the origin and age of
South Mediterranean Provinces (A: p = 0.83; Fig. 4). Within the Asian
Mediterranean plant taxa adapted to arid conditions are still scarce.
clade II dispersal to the Western Mediterranean area occurred only
One of the best studied examples is Haplophyllum (Rubiaceae), a xe‐
for A. syriaca while dispersal to eastern provinces of the ITfr, that is,
rophyte lineage that is distributed in the arid regions from Central
the Turanian or Aralo‐Caspian Province and the Dzhungaro‐Tien Shan
Asia to the Mediterranean basin (Manafzadeh et al., 2014; Salvo
Province, occurred several times. The Mongolian Province was reached
et al., 2011). This genus was used to test whether the ITfr serves
two times; however, apart from A. elatior the identity of these populations
as source for xerophytes to the recipient areas, specifically the
is somewhat unclear (aff. A. aphylla and A. salsa). The Mediterranean/
Mediterranean basin, and indeed, Manafzadeh et al. (2014) found
North African clade spread from Western Mediterranean eastward with
that Haplophyllum originated in the ITfr during the early Eocene,
A. articulata reaching the Egyptian‐Arabian Provinces.
started to diversify during the early Oligocene, and eventually spread
to the Mediterranean region during the middle to late Miocene. Yet,
4 | D I S CU S S I O N
additional xerophytic lineages need to be closely studied to further
verify whether the ITfr is the cradle for arid‐adapted taxa of Asia and
North Africa in general (Manafzadeh et al., 2014, 2017). The results
The ITfr has been suggested to be the geographical origin of, for ex‐
of the current study emphasize that Anabasis is particularly interest‐
ample, the family Brassicaceae (Franzke et al., 2011; Karl & Koch,
ing, because it extends over the whole arid and semi‐arid regions
F I G U R E 4 Time‐calibrated tree generated in BEAST2 of 24 taxa of Anabasis allowing one accession for all monophyletic species and
two accessions for the diphyletic species with disjunct distribution areas (A. oropediorum, A. salsa, A. aphylla, and A. jaxartica). The ancestral
area analysis was conducted using BioGeoBEARS in R v3.3.2. (a) Southern Moroccan Province, Southwestern Mediterranean Province,
South Mediterranean Province; (b) Saharan Province; (c) Northern part of Sudano‐Zambezian Region; (d) Egyptian‐Arabian Province; (e)
Mesopotamian Province, Armeno‐Iranian Province, Hyrcanian Province; (f) Turkestanian Province, Northern Baluchistanian Province,
Western Himalayan Province; (g) Turanian or Aralo‐Caspian Province, Dzhungaro‐Tien Shan Province; and (h) Mongolian Province (see also
Table 1)
|
LAUTERBACH ET AL.
A
g
A. prostrata 1227
A B A. oropediorum 1767
a
f
e
20 3.22
23 1
d
b
B D A. articulata 2359
21 1.88
c
17
A
A. oropediorum 2370
22 1.02
A Southern Moroccan Province,
Southwestern Mediterranean Province,
South Mediterranean Province
F Turkestanian Province,
Northern Baluchistanian Province,
Western Himalayan Province
A B A. aretioides 2424
B Saharan Province
G Turanian or Aralo-Caspian
Province, Dzungaro-Tien Shan
Province
E
C Northern part of Sudano
-Zambezian Region
A D
8
A. syriaca 1468
E F A. haussknechtii 1842
5.46
2.95
H Mongolian Province
D Egyptian-Arabian Province
C3
Mediterr./N. African clade
h
9
13
18
H
E Mesopotamian Province,
Armeno-Iranian Province,
Hyrcanian Province
A. aff. aphylla 2411
C2
19 0.9
H
A. aff. salsa 2413
G
A. ebracteolata 2538
14
1
A
A E
E
H
8
6
5
H
10
4
G
H
H
9
8
5
17 0.53
E G
C E
D E
H
G H
G H
7
5
5
9
E F
C D
D F
C F
G H
G H
G H
G H
12
12
9
7
5
5
E
C E
D E
C D
E F
G
G
G
F G
G
8
8
8
7
6
D E
C E
F G
G
F G
11
11
9
C D
C D
D E
C E
C D
E
E F
E G
F G
F G
F G
G
E
8
8
7
7
5
10
C D
C
D
E
E
E
E
25
A
E
32
16
E
G
8
A
E
35
25
A E
E F
G H
H
8
7
5
13
E
A E
H
5
11 2.98
E G A. eriopoda 2434
E
80
A
A. jaxartica 2540
E
A. aff. jaxartica 1849
C D A. lachnantha 1834
E
C1
7 1.94
G
A E
G
5
11
E
96
E F
21
A E
9
A. calcarea 1841
20
E
A. eugeniae 1844
E G
G H
G H
E
H
13
12
11
7
E G A. annua 1838
6 0.61
14
16
E
E G
E F
E
F G
E
H
G H
H
H
G
15
9
7
6
29
25
E
G
17
G
G
48
19
H
53
45
20
A
A
83
15
23
A
B
B
69
18
A B
G
E
53
G
E
E F
F
H
H
H
H
30
15
64
27
9
A
A
53
41
C D
22
A
A
70
30
B
E F
5 2.15
44
E
21
2 5.52
G
G
B
100
18
15
4 3.2
3 4.54
G
A. cretacea 2011
H
A. brevifolia 2361
B
G H A. truncata 2409
B
D
D
6
5
A. setifera 2012
7.0
6.0
5.0
4.0
3.0
2.0
1.0
0.0 my
Asian clade I
7
E
10
G
10
6.43
C D
A E
15
1
12 2.13
G H
E G
G H
G
93
A
G H A. elatior 2541
E G A. aphylla 2743
E G
H
C D
4.2
16 1.22
D E
10
E G A. salsa 2539
15
G H
50
12
7
7
C E
37
9
G
E
G
G H
E G
7
14
E
H
H
13
6
E
G
13
5
E
2
Asian clade II
3
A E
G H
10
|
LAUTERBACH ET AL.
from North Africa to Central Asia, is highly adapted to aridity, and so
three major clades (Asian clades I and II and Mediterranean clade),
is an excellent model taxon to further infer the biogeographic rela‐
our ancestral area analysis indicates that migration between adjacent
tionships of xerophytic elements of the ITfr and its adjacent regions.
areas (except A. syriaca) is the predominant route of dispersal.
Georeferencing of 441 herbarium specimens of Anabasis showed
Interestingly, the biogeography of Haplophyllum (Manafzadeh
that the distribution area of the genus covers large parts of these arid
et al., 2014) shows parallels to Anabasis: Both Haplophyllum and
areas (Figures 2,5). The relatively low total number of Anabasis col‐
Anabasis started diversifying at the very end or shortly after
lections with sufficiently documented localities was compiled by an
the Messinian salinity crisis at the end of the Miocene (Rouchy
exhaustive investigation of the material of 23 herbaria. This clearly
& Caruso, 2006). Also, during the end of the Miocene, Asian
indicates that most of these desert areas are poorly represented in
Zygophyllum (Zygophyllaceae), which is another arid‐adapted el‐
herbarium collections and might partially explain why xerophytes
ement of Central Asia, underwent a burst of diversification (Wu
of the ITfr have been poorly studied. Fifteen of the 28 spp. studied
et al., 2015). This is a remarkable result, because in contrast to
(Table 1) are distributed in the Turanian and Aralo‐Caspian Provinces
Haplophyllum and Asian Zygophyllum, which likely originated in
and the Dzhungaro‐Tien Shan Province (coded as G in Table 1,
the Early Eocene and Early Oligocene, respectively (Manafzadeh
Figures 4,5). This clearly is the area with the highest species diver‐
et al., 2014; Wu et al., 2015), Anabasis is considerably younger (Late
sity of Anabasis. The Mesopotamian/Armeno‐Iranian/Hyrcanian
Miocene). Additionally, at least Anabasis and Haplophyllum show an
Provinces (coded as E in Table 1, Figures 4,5) are with the occurrence
Eastern and Western Mediterranean divergence dating to the end
of ten different species the second most diverse area. Both areas are
of the Miocene. While Haplophyllum possibly used a northern route
part of the ITfr. The genus occurs in most areas adjacent to the ITfr,
through the Mediterranean basin to reach the Iberian Peninsula
namely the Mediterranean (five spp. in areas A and B), the Saharo‐
(not a southern route via North Africa and Gibraltar; Manafzadeh
Arabian (five spp. in C and D, including the outgroup A. ehrenbergii),
et al., 2017), this seems unlikely for Anabasis since there are no oc‐
and the Mongolian Province (three species in H; Table 1, Figures 2,5).
currences in northern parts of the Eastern Mediterranean, Anatolia,
While most species are restricted to one or two floristic provinces,
and the Balkans. Within the Mediterranean/North African clade of
only two species, A. setifera (Figure 5a: violet squares) and A. syriaca
Anabasis, the best fit model, DEC, suggests an expansion in North
(Figure 5b: rosé circles), are distributed in more than two floristic
Africa from the ancestral area in the west back toward the east
provinces. The ancestral range estimation includes 21 out of 28 spe‐
with the A. articulata/A. oropediorum lineages reaching the Saharo‐
cies. Anabasis ehrenbergii is excluded as its position as sister to the
Arabian region during the Pleistocene (Figures 4, 5c). In addition to
remainder of Anabasis (Figure 3, Supporting Information Appendix
the migration events in the western distribution area of Anabasis,
S4) is questioned by tree topologies resulting from nuclear data sets
it spread also eastwards into the adjacent floristic provinces and
(Schüssler et al., 2017). For seven species (Table 1), the available
reached the easternmost part of the distribution area of Anabasis,
material was either too scarce or not suitable to extract DNA of
the Mongolian province, likely three times (1. A. elatior, 2. a putative
sufficient quality. The missing species are mainly distributed in the
new taxon A. aff. salsa and A. aff. aphylla, and 3. A. brevifolia and
Turanian and Aralo‐Caspian Provinces and the Dzhungaro‐Tien Shan
A. truncata). While A. elatior is a very young element (<0.5 mya) of
Province. Our ancestral range reconstruction does not reveal any
the Mongolian province, A. brevifolia and A. truncata are much older
particular floristic region as the most probable ancestral range for
(95% HPD stem ages: 5.0–1.1 mya and 6.3–1.5 mya, respectively;
Anabasis. Instead, the modern Anabasis lineages seem to have origi‐
Figure 3, Supporting Information Appendix S4). Anabasis brevifolia
nated from within a widespread ancestor within Salsoleae. However,
is an ecologically important species and co‐occurs with Sympegma
due to lack of resolution in the phylogenetic trees (Schüssler et al.,
regelii Bunge as a common and widespread desert dwarf‐shrub
2017 and this study) the closest relative of Anabasis in the tribe re‐
community on shallow and stony soils in the southern Gobi. Both
mains unknown, making it currently impossible to reconstruct the
species belong to the most conspicuous semi‐desert and desert
ancestral area of Anabasis with certainty. While the ancestral area
elements of Central Asia, tolerating extreme drought (Kürschner,
of the Asian clade I was reconstructed as Irano‐Turanian (either E
2004).
or EG or EH; Figures 4, 5a), the common ancestral area of the Asian
Haplophyllum is one of the several examples in which the ITfr
clade II and the Mediterranean clade (clade 3) was reconstructed as a
served as a donor region for its neighboring regions (reviewed
disjunct area involving the Western Mediterranean and the western
in Manafzadeh et al., 2017). The same is true for Anabasis.
Irano‐Turanian (areas A and E; Figure 4: nodes 2 and 8, Figure 5b).
Although the very early biogeographical history of Anabasis re‐
This could reflect a widespread origin and subsequent fragmenta‐
mains somewhat ambiguous with the possibility of a widespread
tion of the ancestral distribution during the Late Miocene. Within the
(Western Mediterranean to Irano‐Turanian) ancestor and area
F I G U R E 5 Distribution areas of Anabasis clades. (a) Asian clade I: A. annua (black squares), A. brevifolia (dark blue squares), A. cretacea (red
squares), A. eugeniae (orange squares), A. lachnantha (white squares), A. setifera (violett squares), and A. truncata (yellow squares). (b) Asian
clade II: A. aphylla (dark blue circles), A. aff. aphylla (light blue circles), A. calcarea (violet circles), A. ebracteolata (dark green circles), A. elatior
(yellow circles), A. eriopoda (black circles), A. hausknechtii (neon green circles), A. jaxartica (white circles), A. salsa (orange circles), A. aff. salsa
(red circles), and A. syriaca (rosé circles). (c) Mediterranean/North African clade: A. aretioides (green triangles), A. articulata (red triangles),
A. oropediorum (blue triangles), A. aff. oropediorum (light blue triangles), and A. prostrata (yellow triangles)
LAUTERBACH ET AL.
(a)
(b)
(c)
|
11
Clade 1 – Asian clade I
stem age 5.07 mya (95% HPD 11.0 – 3.1 mya)
most likely ancestral area: E (p = 14)
(Mesopotamian, Armeno-Iranian,
Hyrcanian Provinces)
Clade 2 – Asian clade II
stem age 4.5 mya (95% HPD: 7.3 – 2.0 mya)
ancestral area: E (p = 32) (Mesopotamian,
Armeno-Iranian, Hyrcanian Provinces)
Clade 3 – Mediterranean /North African clade
stem age 4.5 mya (95% HPD: 7.3 – 2.0) mya
ancestral area: A (p = 83) (Southern Moroccan Province)
12
|
LAUTERBACH ET AL.
fragmentation during the Late Miocene, the ITfr appeared to be
of the ITfr, Anabasis diversified during the late Miocene spread into
source area of xerophytic elements for the neighboring regions,
the adjacent arid biomes of Asia and North Africa. As has been
for example, for the Mediterranean area in case of A. syriaca,
shown for Haplophyllum, the ITfr was identified as cradle for some
which spread from the western ITfr to Morocco, and for the
arid‐adapted taxa of Asia and North Africa, if it is also a sink area
Saharo‐Arabian in case of A. setifera as well as for the Mongolian
for the arid‐adapted lineage Anabasis remains ambiguous. The pro‐
region in case of A. elatior. There is no case in which the ITfr is
posed hypothesis that the expansion of Anabasis coincides with the
an unambiguous sink area. Anabasis is nested within Salsoleae, a
spread of arid and semi‐arid biomes in Eurasia needs to be rejected.
species‐rich tribe consisting of drought‐adapted genera forming
Anabasis did not follow aridification and continuously expanded its
a monophyletic lineage with Caroxyleae and Camphorosmeae,
distribution area, in fact its ancestral distribution area seems to have
which are also mainly xerophytic (Akhani, Edwards, & Roalson,
been fragmented during the very Late Miocene and the remnant lin‐
2007; Kadereit & Freitag, 2011; Kadereit et al., 2012; Schüssler
eages then expanded into neighboring arid regions.
et al., 2017). We assume that the common ancestor at the stem
of the genus (excl. A. ehrenbergii), which dates back to 6.88
mya (95% HPD: 12.1–3.5 mya), was already adapted to drought
and maybe widespread in more arid regions of the Southern
AC K N OW L E D G M E N T S
We thank Rüdiger Masson for generating part of the sequence
Mediterranean area and Asia in the Late Miocene, because during
data and his careful taxonomic study of the Anabasis specimens.
the Late Miocene and Early Pliocene, arid biomes were already
We thank Helmut Freitag for material and helpful advice at the be‐
present in their entire present‐day distribution area including the
ginning of the project. Financial support came from the excellence
relatively young deserts of North Africa (Schuster et al., 2006;
cluster GEOCYCLES. The study of AS is supported by the grant of
Zhang et al., 2014). Morphological, anatomical, and physiological
Russian Fond for Basic Research (project 18‐04‐00029). We are
traits of Anabasis suggest that this genus is highly specialized to
grateful to Nicholas Matzke for help with biogeographic analyses.
survive in arid and saline conditions but probably not competitive
We are grateful to the staff of the following herbaria; B, BCN, BEI,
under more mesic conditions. Except for A. annua—a therophyte,
BM, E, GLM, HAL, K, KAS, LE, M, MJG, MO, MPU, MSB, MW, P,
which, however, is a derived character within the genus—the rest
STU, TARI, TUH, UPS, W & WU for providing loans of Anabasis
of Anabasis species are very slow‐growing stem‐succulent shrubs
specimens (for information of herbarium acronyms, see Thiers,
with reduced or barely developed leaves and little amounts of
2018). We thank Maria Geyer for help with the illustrations.
putatively highly efficient photosynthetic tissue performing C4
photosynthesis (Schüssler et al., 2017; pers. observation). Several
species are able to resprout (e.g., Bokhari & Wendelbo, 1978;
Fahn & Dembo, 1964; Olufsen, 1912; Sukhorukov & Baikov,
2009; Voznesenskaya, 1976a,b; pers. observation). Studies of
the reproductive organs of Chenopodiaceae show that Anabasis
DATA AC C E S S I B I L I T Y
Genbank
accessions
MF156717‐MF156846
and
MF580497‐
MF580548 (for further information see Supporting Information
Appendix S1).
seeds have large, green, coiled embryos without nutritive tissue
that is in agreement with the seed structure of other Salsoloideae
(Sukhorukov, 2008; Sukhorukov et al., 2015) having very fast ger‐
mination (Kadereit et al., 2017 and ref. therein). Climate change
was shown to differently affect regions of the world (Kirtman
et al., 2013). For the ITfr, it was projected that the effects will
vary depending on the location within the ITfr: precipitation will
increase in some parts of the ITfr, whereas it will decrease in
AU T H O R C O N T R I B U T I O N S
M.L. and G.K. designed the study; M.L. performed the molecular
work, edited and aligned sequences; M.L. and M.V. performed the
analyses, M.L. and G.K. wrote the draft of the manuscript; M.L, M.V.,
A.S., and G.K. revised the manuscript; and all authors contributed to
the final version of the manuscript.
other parts (Kirtman et al., 2013; Manafzadeh et al., 2017). The
slow‐growing Anabasis is highly specialized in arid habitats and
ORCID
likely is at a competitive disadvantage under more mesic condi‐
https://orcid.org/0000‐0002‐9450‐5485
tions (see above). Thus, arid‐adapted lineages of the highly di‐
Maximilian Lauterbach
verse ITfr in general and Anabasis in particular are threatened by
Marie Claire Veranso‐Libalah
climate change at least in the parts of the ITfr that will experience
org/0000‐0001‐7847‐1740
https://orcid.
higher precipitation in the future, and because of that the conser‐
vation of those ITfr habitats needs to be prioritized.
In summary, an extensive sampling of Anabasis (21 out of 28 spe‐
cies included in the molecular analyses) revealed the complex bioge‐
ography of the genus and showed that species occurring in the same
floristic region do not form monophyletic groups but are a mosaic of
old and young lineages of this genus. Like other xerophytic elements
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section at the end of the article.
How to cite this article: Lauterbach M, Veranso‐Libalah MC,
Sukhorukov AP, Kadereit G. Biogeography of the xerophytic
genus Anabasis L. (Chenopodiaceae). Ecol Evol. 2019;00:1–14.
https://doi.org/10.1002/ece3.4987