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Botanical Journal of the Linnean Society, 2013, 171, 201–224. With 6 figures
Historical biogeography and life-history evolution of
Andean Puya (Bromeliaceae)
RACHEL S. JABAILY1,2* and KENNETH J. SYTSMA1
1
2
Department of Botany, University of Wisconsin, Madison, WI, USA
Department of Biology, Rhodes College, Memphis, TN, USA
Received 6 December 2011; revised 14 August 2012; accepted for publication 27 August 2012
Puya (Bromeliaceae), with > 200 species, is a classic example of a recent, rapid species-level radiation in the Andes.
To assess the biogeographical history of this primarily Andean species group and the evolution of different life
histories, amplified fragment length polymorphism (AFLP) data were generated for 75 species from throughout the
geographical range of the genus. Distribution data for latitudinal and elevational ranges were compiled for almost
all species. The greatest number of species is found at mid-elevations and mid-latitudes south of the equator. The
genus originated in central Chile and first moved into the Cordillera Oriental of the central Andes via inter-Andean
valleys. Cladogenesis progressed in a general south to north direction tracking the final uplift of the Andes. All taxa
north of the Western Andean Portal form a monophyletic group implying a single colonization of the northern
Andes, with no subsequent transitions back south from the Northern Andes. Repeated evolutionary transitions of
lineages up and down in elevation are suggestive of allopatric speciation driven by Pleistocene glaciation cycles.
True semelparity evolved once in P. raimondii, with similar semi-semelparity evolving repeatedly in páramos of the
northern Andes. Fieldwork and phylogenetic characterization of high-elevation Puya are priorities for future
efforts. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224.
ADDITIONAL KEYWORDS: AFLP – BayesTraits – elevation – latitude – monocarpic – semelparity –
Western Andean Portal.
INTRODUCTION
Understanding evolution in the Andes, the most
extensive mountain system on earth, is both fascinating and challenging due to the impact of extensive
recent geological upheavals on the biota and the difficulties involved in elucidating relationships between
the large number of species found within this complex
geographical space, which are often of recent origin.
The tropical latitudes of the Andes are the most
important biodiversity hotspot on the planet, in terms
of both number of species and levels of endemism
(Luteyn, 1999; Myers et al., 2000; Young et al., 2002).
The Andes are home to rapid and extensive plant and
animal species radiations (Smith & Sytsma, 1994;
Cardillo, 1999; Berry et al., 2004; Bell & Donoghue,
2005; Kay et al., 2005; Fjeldsa & Rahbek, 2006;
Hughes & Eastwood, 2006; Drummond, 2008; Scher*Corresponding author. E-mail: jabailyr@gmail.com
son, Vidal & Sanderson, 2008; Jabaily & Sytsma,
2010; Chaves, Weir & Smith, 2011; Givnish et al.,
2011; Sklenář, Dušková & Balslev, 2011). The extent,
recent evolution and high rates of species diversification found for several species-rich Andean plant
groups [e.g. Lupinus L. (Hughes & Eastwood, 2006;
Drummond, 2008; Drummond et al., 2012), Valeriana
L. (Bell & Donoghue, 2005; Moore & Donoghue, 2007),
core Tillandsioideae (Givnish et al., 2011)] and the
uniquely steep and extended latitudinal and altitudinal gradients found in the Andes highlight this region
as an ideal study system for investigating plant diversification (e.g. Särkinen et al., 2011). Understanding
why the Andes are rich in species remains a key
challenge in Neotropical biology (Rull, 2011). A more
thorough understanding of the processes involved in
making the Andes so rich in species can also help
inform more broadly the mechanisms behind the
genesis and maintenance of extensive species-level
radiations.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
201
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R. S. JABAILY and K. J. SYTSMA
Geologically driven allopatric speciation with subsequent differentiation and/or parapatric ecological
speciation along habitat gradients are the main evolutionary scenarios postulated for many Andean
animals and plants (Gentry, 1982; Young et al., 2002;
Brumfield & Edwards, 2007). However, detailed
studies involving these cladogenic processes in the
Andes and the Neotropics are more common in vertebrates than in plants to date (Young et al., 2002;
Hall, 2005; Weir, 2006; Brumfield & Edwards, 2007;
Ribas et al., 2007; Torres-Carvajal, 2007; Elias et al.,
2009; Santos et al., 2009; Chaves et al., 2011), in part
because of greater baseline field knowledge and collecting efforts in some animal groups compared with
plant groups. Historical biogeographical explanations
for Andean radiations are increasingly based on timecalibrated phylogenies and use of explicit biogeographical models (Richardson et al., 2001; Berry
et al., 2004; Kay et al., 2005; Moore & Donoghue,
2007; Alzate, Mort & Ramirez, 2008; Drummond,
2008; Antonelli et al., 2009; Cosacov et al., 2009;
Givnish et al., 2011; Luebert, Hilger & Weigend, 2011;
Särkinen et al., 2011; Drummond et al., 2012).
The charismatic genus Puya Molina (Bromeliaceae), with > 200 described species of terrestrial
rosette-forming bromeliads (Fig. 1), is a striking
example of recent rapid species diversification in the
Andes, providing an ideal study group to investigate
Andean species radiations (Jabaily & Sytsma, 2010;
Schulte et al., 2010; Givnish et al., 2011). The genus
comprises two major clades, one endemic to lowland
and coastal habitats in central Chile and the other
almost exclusively Andean and spanning all tropical
and significant portions of temperate Andean latitudes. Species are found from sea level to > 4500 m
elevation (Fig. 2) in habitats including high elevation
páramo and puna, mesic and xeric inter-Andean
valleys, portions of the lowland chaco and the coastal
Chilean matorral (Fig. 1). Two species are found in
Panama and Costa Rica, one endemic and one widespread into the northern Andean lowlands. Puya
flowers provide nectar for hummingbirds, the main
pollinators, and are utilized as a food source by the
spectacled bear. Puya fruits produce copious seed with
a small, papery wing appendage but are generally
thought to be poor dispersers. Perhaps as a consequence, many species are narrow endemics, often
found in a single valley. Bromeliaceae are rosetteforming monocots typically with terminal inflorescences that do not continue to grow after flowering
(Benzing, 2000) (Fig. 1). Many bromeliads reproduce
asexually via production of clonal offshoot ramets
(‘pup’ rosettes), which either remain attached to the
mother plant, or sever to produce physiologically
independent individuals. Puya is one of several
genera of Bromeliaceae that vary in the ability of
different species to produce pup rosettes (Barbará
et al., 2009). Most species of Puya are iteroparous (R.
S. Jabaily, pers. observ.) forming large colonies of
attached clonal rosettes, especially in marginal habitats such as rocky cliff faces. A small number of
high-elevation species show reduced ability or even
inability to produce pup rosettes before or after inflorescence production and thus are effectively reproducing only sexually. Puya is also one of the relatively
few lineages of long-lived plants with taxa that are
semelparous (or monocarpic: Young & Augspurger,
1991). The repeated evolution of semelparity particularly in tropical montane ecosystems is a fascinating
case of convergent evolution (Hedberg & Hedberg,
1979; Smith & Young, 1987), and the evolution of this
risky life-history strategy raises many evolutionary
questions that can best be framed in the light of
established phylogenetic relationships between taxa.
An initial phylogenetic analysis of Puya uncovered
two major clades with robust support using a combination of plastid DNA and nuclear single-copy PHYC
gene sequences (Jabaily & Sytsma, 2010), but levels
of informative sequence variation for these loci in the
primarily Andean ‘core Puya’ clade were too low to
resolve species relationships. The family-wide phylogeny of Givnish et al. (2011) used nearly 10 000 bp of
plastid sequence, but phylogenetic resolution between
the eight sampled species of Puya (beyond retrieval
of the two major clades) was minimal, in line with
known low rates of sequence evolution in the family
as a whole (Gaut et al., 1992; Givnish et al., 2007;
Smith & Donoghue, 2008; Sass & Specht, 2010).
However, Andean bromeliads are by no means
unique, as most published DNA sequence-derived
phylogenetic trees for high-elevation Andean clades
are poorly resolved (e.g. Emshwiller, 2002; Andersson,
2006; Hershkovitz et al., 2006; Alzate et al., 2008;
Soejima et al., 2008; Cosacov et al., 2009).
The use of amplified fragment length polymorphism
(AFLP) provides an alternative to direct sequencing for species-level phylogenetics particularly for
recent and rapidly radiating groups (Albertson et al.,
1999; Després et al., 2003; Richardson et al., 2003;
Koopman, 2005; Spooner, Peralta & Knapp, 2005;
Pellmyr et al., 2007; McKinnon et al., 2008; Dasmahapatra, Hoffman & Amos, 2009; Kropf, Comes &
Kadereit, 2009; Arrigo et al., 2011; Bacon et al., 2011;
Gaudeul et al., 2012). Despite the often mentioned
advantages and limitations of using AFLP in phylogenetic analyses (see recent review by Gaudeul et al.,
2012), few studies have explicitly assessed congruence between phylogenetic analyses based on AFLP
and DNA sequence data or provide a theoretical basis
for using or not using AFLP. Importantly, recent theoretical studies indicate that the major drawback of
this technique is the low information content of AFLP
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
A
B
C
D
203
E
Figure 1. Habitats and life forms of Puya species. A, P. ferruginea (Ruiz & Pav.) L.B.Sm., Cusco, Peru. B, P. compacta
L.B.Sm., Azuay, Ecuador. C, P. raimondii Harms, Ancash, Peru. D, P. exigua Mez, Azuay, Ecuador. P. alpestris Poepp.,
Coquimbo, Chile. Photos: A–D, R. S. Jabaily; E, M. J. Jabaily.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
204
R. S. JABAILY and K. J. SYTSMA
10°
5°
N
0°
S
5°
Latitude
10°
15°
20°
25°
30°
35°
40°
0
500
1000
1500
2000
2500
3000
3500
4000
4500
Elevation
Figure 2. Latitude and elevation ranges for individual species of Puya (Bromeliaceae). Species ranges known only from
type specimens are represented as a dot or a line; species with multiple collections are depicted as boxes with the
dimensions corresponding to known latitude and elevational limits.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
markers (Simmons et al., 2007; García-Pereira,
Caballero & Quesada, 2010, 2011) and not the other
commonly invoked limitations such as the lack of
homology of co-migrating fragments (García-Pereira
et al., 2010), the dominant nature of AFLP characters
(Simmons et al., 2007) and correlation with genome
size (Fay, Cowan & Leitch, 2005; Althoff, Gitzendanner & Segraves, 2007; Caballero & Quesada, 2010).
Recent studies on the effectiveness of AFLP markers
indicate that they are appropriate for phylogenetic
inference as long as sequence divergence is low, the
topology of the underlying evolutionary tree is not
strongly asymmetric and basal nodes do not have
short branch lengths (García-Pereira et al., 2011).
Under certain circumstances, AFLP may be suitable
to reconstruct even deeper phylogenies than usually
accepted (García-Pereira et al., 2010). Current evidence also suggests that AFLPs largely behave as
neutral characters (Bonin, Ehrich & Manel, 2007) and
that an AFLP-based clock may be appropriate with
shallow divergences (Kropf et al., 2009).
AFLPs have been used at both the population and
the species level in Bromeliaceae (Sgorbati et al., 2004;
Rex et al., 2007) and in other Andean plant groups for
which lack of DNA sequence variation is also an issue
(Tremetsberger et al., 2006; Schmidt-Lebuhn, Seltmann & Kessler, 2007; Emshwiller et al., 2009; Nakazato & Housworth, 2011). Schulte et al. (2010) explored
the utility of AFLP at both the interspecific and the
intrapopulation level in the ‘Chilean Puya’ clade to
determine relationships between species and detect
putative hybrid individuals. In this study the AFLPbased analyses supported species monophyly (except
for noted hybrid individuals) and were congruent with
the main phylogenetic divisions in Puya based on
nuclear and plastid DNA sequence data (Jabaily &
Sytsma, 2010). Thus there is evidence to suggest that
AFLP data can be used to provide a reasonable estimate of species relationships, at least in Puya.
The goals of this study were to (1) reconstruct a
preliminary phylogenetic framework for Puya with
emphasis on the Andean species of Puya, (2) use this
framework to investigate historical biogeographical
patterns in the Andes and (3) analyse patterns in
life-history (reproductive strategy) variability and
evolution. To that end, a baseline phylogenetic tree
employing representative sampling of species from all
major Andean regions was generated using a large
AFLP data set. This new framework is combined with
distribution data to investigate the historical biogeography of Puya in the Andes. Specifically, the frequencies of evolutionary transition across latitudinal
and elevational space are quantified under different
analytical models to gain insight into the potential
role of Andean uplift versus glaciation cycles in
driving species diversification.
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MATERIAL AND METHODS
Plant material was collected throughout the Andes
from 2006 to 2008 and from the extensive living plant
collection at the Huntington Botanical Garden (San
Marino, CA, USA). Herbarium material was not used
because of the necessity of high-quality DNA for
AFLP analysis. As many Puya spp. as possible were
observed and collected at localities spanning the geographical range of the genus and including all major
habitats where Puya occurs. In addition, latitudinal
and elevational ranges for 193 of the 214 recognized
species were generated from field data, information
from Smith & Downs (1974) and Manzanares (2005)
and specimen data from herbaria in the USA and
South America (NY, US, F, MO, SEL, WIS, HNT, USZ,
LPB, QCNE, LP, MCNS, CONC, COL, USM, CUZ,
HUT).
AFLP
ANALYSIS
Ninety-eight accessions representing 75 Puya spp., all
identified by the first author, were included in the
AFLP analysis (Appendix 1). These accessions span
the taxonomic, morphological and geographical range
of the genus and included 40 species not sampled in
the previous analysis of Jabaily & Sytsma (2010).
Multiple individuals from multiple populations of 18
species were included to test species monophyly.
Several putative new species from Apurimac, Peru,
were also included. For a subset of accessions and
primer pairs multiple independent AFLP analyses
were performed to test for repeatability of the fragments generated.
AFLP fragment generation and isolation protocols
follow Emshwiller et al. (2009). Total genomic DNA
was extracted with the DNeasy Plant Kit (Qiagen,
Valencia, California) following the manufacturer’s
protocol. All enzymes and buffers used for the entire
AFLP fragment process were from New England
Biolabs (Ipswich, MA, USA). For the initial digestion step, 3.7 mL DNA was digested with 0.5 mL
MseI, 0.25 mL EcoRI (enzyme concentrations were 50
U/mL), 0.5 mL EcoRI buffer and 0.05 mL bovine serum
albumin at 37 °C for 2 h. Immediately after completion of the digestion step, double stranded adapters
were ligated to each digestion product in reactions
with 5 mL digestion product, 1 mL ligase buffer,
0.19 mL each of EcoRI and MseI adaptors, 0.10 mL T4
DNA ligase and 3.52 mL water for a total reaction
volume of 10 mL, held at 16 °C for 14 h.
Before the first round of amplification, 7 mL of
product was diluted with 29 mL of water. The first
round of amplification used primers EcoRI+A and
MseI+C. Reaction mixes used 5 mL of the diluted
digested DNA with attached adaptors, 2.5 mL 10¥
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
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R. S. JABAILY and K. J. SYTSMA
buffer, 2 mL dNTPs, 0.38 mL each primer, 0.25 mL Taq
polymerase and 14.5 mL of water for a total reaction
volume of 25 mL. The cycling regime was 1 min denaturation at 72 °C, followed by 20 cycles of 94 °C for
1 min, 56 °C for 1 min and 72 °C for 2 min, and a final
extension of 72 °C for 2 min. Before the final amplification step, 20 mL of the product was diluted with
360 mL water. A second, more selective round of
amplifications followed with the following primer
combinations (M+CGA/E+ATG, E+AGC, E+AC;
M+CGG/E+ATT; M+CTC/E+AGC, E+AC, E+ATG;
M+CAT/E+AC; M+CCC/E+AC). Reaction mixes for the
second round of amplifications were 5 mL of the
diluted product from the first round of amplifications,
2.5 mL of 10¥ buffer, 3 mL dNTPs, 0.5 mL deionized
Hi-Di formamide (Applied Biosystems, Carlsbad, CA,
USA), 2.5 mL of the MseI primer, 0.5 mL of EcoRI
primer fluorescently labelled with 6-FAM, 0.25 mL
Taq and 10.75 mL water for a total reaction volume of
25 mL. The cycling regime was nine cycles of 94 °C for
50 s, 65 °C for 1 min (decrease by 1 °C per cycle) and
72 °C for 2 min, followed by 20 cycles of 95 °C for 50 s,
56 °C for 1 min, 72 °C for 2 min and a final extension
of 72 °C for 10 min.
PCR products were electrophoresed on an ABI
3700 automated sequencer (Applied Biosystems,
Foster City, CA, USA) with a 500ROX-labelled internal lane standard at the University of WisconsinMadison Biotechnology Center. Output profiles were
visualized and analysed using GeneMarker (SoftGenetics, State College, PA, USA) using the settings of
Holland, Clarke & Meudt (2008). After visual inspection of every profile generated for each accession
from each primer pair, some manual adjustments
were made to the determinations of peaks by the
program.
ROOTING
OF THE PHYLOGENY
A positive relationship between phylogenetic distance
and AFLP homoplasy has been well documented
(Fay et al., 2005; Koopman, 2005; Althoff et al., 2007).
Initially, Ananas Mill. from the sister subfamily
Bromelioideae and the more distantly related Deuterocohnia Mez were included for potential rooting
purposes, but were ultimately discarded because
of suspected non-homology of fragments. For both
outgroup accessions, the number of bands scored as
present was much lower than in Puya (166 for
Ananas, 168 for Deuterocohnia, average 245 for Puya
taxa) and distance analyses found the outgroups to be
more similar to each other than either was to Puya,
which does not coincide with the current understanding of relationships in Bromeliaceae (Givnish et al.,
2011). Rooting of the AFLP phylogeny using non-Puya
outgroups was also deemed inappropriate based on
comparison of sequence similarity at various phylogenetic levels in a nuclear ribosomal internal transcribed spacer (ITS) dataset (data not shown). The
level of ITS sequence divergence between the outgroup genera and Puya was three times higher than
that recommended by Koopman (2005) for application
of AFLP and was in the appropriate range of 10–30
variable nucleotide positions in Puya. Thus, based on
these data and outgroup rooting of the AFLP dataset
indicating relationships not seen with other plastid or
nuclear genes in previous studies, we only included
Puya for AFLP analysis in this study.
Rooting the core Andean Puya phylogenetic tree
using the Chilean clade is also complicated by ancient
plastid introgression that means that almost all taxa
from Chile group with the ‘Chilean Puya’ clade in the
plastid gene tree, generating incongruence between
the plastid DNA and PHYC nuclear gene trees
(Jabaily & Sytsma, 2010). The AFLP topology places
taxa from Chile in two clades, corresponding in composition to the ‘Yellow Puya’ and ‘Blue Puya’ clades
identified through analysis of the low-copy nuclear
region PHYC (Jabaily & Sytsma, 2010). The ‘Blue
Puya’ clade was identified as the sister to all other
Puya in this former analysis based on nuclear DNA.
Issues of gene tree/species tree discordance are potentially avoided by analysing hundreds of AFLP fragments (Giannasi, Thorpe & Malhotra, 2001), which
effectively span the nuclear genome (Althoff et al.,
2007). Given the primary focus of the AFLP analyses
presented here on non-Chilean Andean Puya, the
‘Blue Puya’ clade was used as the functional outgroup
(the sister group to all other Puya) for all subsequent
analyses.
PHYLOGENETIC
ANALYSES
The resultant AFLP presence/absence matrix was
analysed using distance and Bayesian inference.
Neighbour-joining (NJ) trees were calculated in
PAUP*4.0b10 (Swofford, 2002) using the Nei–Li distance matrix, minimum evolution, NJ start tree and
TBR branch swapping. A consensus network was constructed using NeighborNet (Bryant & Moulton,
2004) to visually assess non-bifurcating events and
conflicting phylogenetic signal. Nei–Li distances (Nei
& Li, 1979) were generated and analysed in the
program SplitsTree4, version 4.12.4 (Huson & Bryant,
2006).
Genetic distance methods are often employed for
analysis of AFLP and other restriction-site data,
but converting all the data into pairwise distance
measurements may cause a loss of information
and uncertainty in the topology is not conveyed. We
thus implement model-based methods that provide
topologies with branch lengths that can be used
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
in BayesTraits (Pagel, Meade & Barker, 2004) for
subsequent character analyses. Likelihood-based
methods for analysing AFLP data include a simple
binary data/restriction site model implemented in
MrBayes 3.1 (Ronquist & Huelsenbeck, 2003) and the
more sophisticated model specifically designed for
AFLP data of Luo, Hipp & Larget (2007). This newer
model takes into account the length of restriction
sites and the possibility of substitutions or indels in
the interior of fragments. Unfortunately, the method
is currently computationally costly and analysis of a
dataset this size was computationally intractable (B.
Larget, pers. comm.). The model of restriction site
evolution implemented in MrBayes, although perhaps
overly simplistic in its assumptions of restriction site
gain and loss, approximates the gain and loss of
fragments. The dataset was analysed with two independent runs in MrBayes using the prior settings
Dirichlet (2.65, 1.00) (lset coding = noabsencesites)
and an MCMC run of 120 000 000 generations, samplefreq = 5000 and the default setting to discard the
first 25% of runs as burn-in. Convergence and stationarity of the MrBayes analysis were determined by
evaluating the standard deviation of split frequency
values at the end of the run, a plot of the generation
vs. log likelihood values and the potential scale reduction factor convergence diagnostic.
For subsequent biogeographicaql analyses in which
bifurcating trees were required, the program
Summary Tree Explorer (Derthick, 2008) was used to
generate a priority-rule consensus tree from 2000
randomly chosen trees from the post burn-in MrBayes
output. The priority-rule consensus tree allows for
clades with < 50 posterior probability if not in conflict
with other clades.
HISTORICAL
BIOGEOGRAPHY
The geographical distributions of taxa included in the
AFLP dataset were scored as present or absent in
three different categories of geographical space: (1)
discrete Andean cordilleras sensu Simpson (1975) –
Coastal, Principal, Pampean, Oriental, Occidental,
Western Colombian Andes, Central Colombian Andes,
Eastern Colombian Andes; (2) broad latitudinal belts;
and (3) broad elevational belts. The latter two categories were analysed as three- and two-state area
codings. For scoring of broad latitudinal belts, the
break between northern and central/southern Andes
was placed at the Western Andean Portal/Rio
Marañon Valley/Amotape-Huancabamba deflection
zone (hereafter WAP, following Antonelli et al., 2009),
located between 3 and 5°S. For the two-state latitude
analysis, species were coded as present north or south
of the WAP. For the three-state latitude analysis,
species were coded as north of the WAP, between the
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WAP and the Tropic of Capricorn or south of the
Tropic of Capricorn. For the two-state elevational
analysis, taxa were scored as low-elevation if found
below 3000 m and high elevation if found above
3000 m. For the three-state coding, taxa found at
0–1500 m were coded as low elevation, taxa at 1500–
3000 m as mid elevation and taxa at ⱖ 3000 m as
high elevation.
The three sets of discrete biogeographical characters were mapped onto the priority-rule Bayesian
inference phylogeny using several methods. First,
ancestral state was reconstructed under the
maximum parsimony (MP) criterion using the
program MESQUITE (Maddison & Maddison, 2008).
All possible ancestral reconstructions were examined.
Character homoplasy was assessed with the consistency and retention indexes (CI, RI; Felsenstein,
1978).
Second, we employed ancestral state reconstruction
using the MultiState program implemented in
BayesTraits ver. 1.0 (Pagel et al., 2004). Although
phylogenetic analyses based on AFLP data typically
only involve assessment of topology and support,
AFLP branch length information was used by Whittall & Hodges (2007) to model character evolution in
Aquilegia L. More recently, Kropf et al. (2009) documented a linear relationship between the degree of
AFLP divergence and time of isolation in three unrelated species of alpine plants and advocated the use of
an AFLP-based clock for absolute dating. We explored
the AFLP trees using more explicit model-based
approaches offered in BayesTraits. For these analyses
2000 rooted phylogenies chosen at random from the
post-burnin MrBayes analyses were used and the
data were first optimized under a maximumlikelihood (ML) framework to find the parameters and
likelihood scores in order to inform the subsequent
Bayesian inference analysis. This analysis was run in
a reverse-jump MCMC framework with rate coefficients drawn from an exponential (0–10) hyperprior
distribution. The transition rate parameter (ratedev)
was adjusted until the acceptance values averaged
20–40%, as recommended (Pagel & Meade, 2006). The
number of generations and priors were adjusted to
minimize differences between the average log likelihood and the log likelihood from the initial ML run,
minimize change across runs in the harmonic mean
and have an appropriate average ratedev. Each analysis was run twice with 10 000 000 iterations per run,
the first 2500 000 discarded as burn-in and trees were
sampled every 1000 iterations. Outputs from the two
runs were combined and the average probabilities of
the character states for each character were determined for each of the analysed ancestral nodes. Likelihood ratio tests were performed to assess the
significance of transition rate values and test various
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R. S. JABAILY and K. J. SYTSMA
hypotheses of character evolution (Pagel & Meade,
2006). Analyses were conducted in a likelihood framework and the average log-likelihood value was compared between analyses using the likelihood ratio test
statistic.
Third, we utilized the program S-DIVA (Yu, Harris
& He, 2010) using just the Andean cordilleran dataset
to reconstruct past dispersal and vicariance events in
Puya while incorporating uncertainty in the underlying phylogeny. The Andean cordillera dataset was
optimized across the same 2000 randomly chosen
phylogenies analysed in BayesTraits. Constraining
ancestral areas to two, three or four cordilleras was
explored, as well as the impact of restricting ancestral
areas to cordilleras that are currently adjacent.
In addition to these three approaches to reconstruct
the biogeographical history of species diversification
in Puya, we also assessed the degree of correlated
elevational and latitudinal transitions across the phylogeny of Puya using binary characters for both elevation and latitude. The degree of potential covariance
of changes in the two-state elevation and latitude
datasets was assessed in a phylogenetic framework
using the Discrete program in BayesTraits (Pagel &
Meade, 2006). This program evaluates two models,
the first in which elevation and latitude evolve independently on the tree. This creates two rate coefficients per trait or four rate coefficients that must be
estimated. The second model allows the traits to
evolve in a correlated fashion such that the rate of
change in one trait depends on the background state
of the other. The dependent model has four states, one
for each combination of the two binary traits or eight
rate coefficients that must be estimated. A likelihood
ratio test with four degrees of freedom was used to
determine if a dependent or independent model of
character evolution was favoured by the data.
LIFE-HISTORY
EVOLUTION
We also examined life-history transitions across the
Puya phylogeny. Three life-history types (Table 3)
were scored for all accessions of Puya: 0 = iteroparous,
1 = semi-semelparous and 2 = semelparous. Transitions between any pair of states were allowed. This
character was analysed in BayesTraits MultiState
using the same subset of phylogenies and parameters
as for biogeographical data.
RESULTS
PATTERNS
OF DISTRIBUTION IN LATITUDE
AND ELEVATION
Puya spp. are found throughout the Andes from sea
level to > 4500 m, at latitudes from 40°S to 10°N, but
species diversity is not evenly distributed across these
geographical axes (Figs 2, 3). The greatest numbers of
species are found at mid elevations and mid latitudes,
and the majority of these have relatively restricted
latitudinal and elevational ranges. Low-elevation
species (1500 m and below) are most common at the
southernmost latitudes, but are found to a limited
extent scattered across all latitudes, and these species
tend to have wider latitudinal ranges than highelevation species. High-elevation species (3000 m and
above) are rare south of the Tropic of Capricorn.
Species found north of the Equator tend to inhabit
high elevations and have smaller latitudinal and
elevational ranges, with the exception of the widespread P. floccosa E.Morren ex Baker. Nearly onethird of the species are known only from single (type)
localities. Species numbers increase with elevation,
with > 40 species found between 2600 and 3300 m,
followed by a decline in species number at higher
elevations. The highest numbers of species are found
at several central Andean latitudes (9°S, 17°S), with
species number decreasing both north of the equator
and south of the Tropic of Capricorn. When distribution across latitudinal space was depicted as distance
from the equator (e.g. the number of species found at
5°N and 5°S were added together to give the number
of species 5° from the equator), the increase in species
number towards the equator is roughly linear (Fig. 3).
A standard R2 linear regression found a moderately
good fit of the data to a linear model (R2 = 0.725).
PHYLOGENETIC
ANALYSES
Both distance and Bayesian inference methods were
used to analyse the 885 AFLP fragments generated.
Fragments generated from independent rounds of
laboratory work from the same DNA samples were
nearly identical. The resultant topologies from the
two analyses were highly congruent, as was the
overall topology of the NeighborNet analysis (Fig. 4).
In this latter analysis, taxa resolve into four major
clusters, corresponding to the clades ‘Central &
Northern Andes’, ‘Central & Southern Andes’, ‘Zygomorphic’ and ‘Blue Puya’. Puya aequatorialis André
and P. atra L.B.Sm. were placed in an intermediate
position relative to the two largest clusters.
In the Bayesian inference phylogeny (Fig. 5), rooted
with the functional outgroup ‘Blue Puya’ (Chilean
species with blue flowers), a well-supported [posterior
probability (PP) 97] clade comprising the widespread
P. ferruginea (Ruiz & Pav.) L.B.Sm. and the narrow
endemic P. mima L.B.Sm. & Read is placed as sister
to the remainder of the genus. These two species
both have large zygomorphic flowers (Fig. 1A). The
remaining Puya spp. are placed in two main wellsupported sister clades: a Central & Northern Andes
clade (PP 96) and a Central & Southern Andes clade
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
209
BIOGEOGRAPHY OF PUYA
A
40
35
30
25
20
15
10
Number of species present
45
5
0
0
500
1000
1500
2000
2500
3000
3500
4000
4500
5000
Elevation (meters)
B
16
12
10
8
6
4
Number of species present
14
2
0
-40
-35
-30
-25
-20
-15
-10
-5
0
5
10
Latitude (degrees from the equator)
Figure 3. Numbers of species of Puya with ranges at A, each 100 m of elevation and B, each 0.5 degree of latitude.
Negative values are south of the equator, positive north of the equator. Black dots correspond to presence by latitude from
the equator irrespective of hemisphere, and are therefore additive from -10 to 0; grey dots correspond to latitudinal
position in both hemispheres.
(PP 100). Puya atra L.B.Sm from central Bolivia is
sister to the remainder of a Central & Northern
Andes clade (PP 98), which form two subclades. The
‘Yellow Puya’ clade (Chilean taxa with yellow flowers)
is nested in a well-supported (PP 100), primarily
high-elevation clade from both the Cordilleras Occidental and Oriental composed of P. yakespala A.Cast.,
P. herrerae Harms, P. angusta L.B.Sm., P. weberbau-
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
tia
n
a
P.
go
ud
otia
P.
na
tria
na
P.
e
tria
na
e
P.s
a
ou
do
es
P.
ni
tid
a
P.g
ides
a
id
ii
nit
os
P.
nt
sa
P.
lor
o
bic
P.
ata
ine
P.l
P.a
ea
alis
tori
ua
eq
yg
ma
a
P.h
P.d
a
P.
P. mac
ha
m ulat
at
a a
ta
P.p
ae
syli
rioid
ii
en
mp
ac
ylirio
ns
co
P.p
ygm
P.da
s
na
e
va
ea
e
rg
joe
P.
e
cu
P.
P.raim
ondii
P.rai
mon
dii
P.tillii
P.exigua
na
asia
ros
P.
P.eryngioides
a
irtzii
na
P.
P.nitida
P.h
oa
hom
P.t
arr
av
ns
ta
nu
P.
l
tra
n
e
C
rs
P.retro
P.n
a
iroan
P.sod
dii
plun
P.as
des
rn An
e
h
t
or
&N
nto
sii
R. S. JABAILY and K. J. SYTSMA
P.parviflo
ra
210
am
ata
P.c
aja
sen
P.ob
a
ian
ron
sis
erte
P.b
a
e Puya
Blu
conic
tris
lpes
P.a
P.yake
spala
P.herre
estris
P.alp
stris
P.alpe
rae
P.angusta
P.angusta
ea
P.coerul
P.coerulea
P.weberbaueri
P.venusta
is
P.casmichens
P.venusta
P.venusta
P.coeru
is
P.chilens
lea
P.coer
ul
ea
iae
artin
Ye l l o
is
ens
il
h
P.c
w
Pu
sis
ilen
P.ch
P.m
ima
sis
is
ien
ns
oliv
vie
P.b
oli
P.b
P.fe
rr
ugin
ugin
P
ea
P.f
err
ya
sp
s
P.
ae
p
yr
ine
a
ta
na
la
P.
ht
ii
rig
w
a
im
ult
P.
ei
arc
de
ns
iflo
ra
Z
P.laxa
P.vasquezii
rosa
sis
nden
P.tube
lo-gra
P.val
P.claudia
e
cis
noth
P.sa
ncta
e-cru
P.s
te
P.n
ana
rys
a
pe
P.
s
ide
kio
yc
ez
lii
a
ce
bilis ilis
ira
ab
P.m P.mir
loi
P.lil
cea
atha
P.sp
P.d
9
21
P.
SJ
1
ii
va
oli
P.
s
sii
no
lla
rm
ha
ste
ca
P.
22
err
ug
ine
a
es
P.dyckioid
ens
P.micrantha
arae
P.nov
rg
P.assu
C en
P.
ro
RS
J
R
P.
rre
fe
P.
P.
m
P.
ug
P.f
a
ur
r
ac
P.
ea
P.fe
rr
a
r
.at
o m or p hi c
P.gilm
yg
nsis
P.chile
tral & Souther n Andes
Figure 4. Phylogenetic network of 98 Puya accessions from 75 species based on NeighborNet analysis of Nei–Li distances
generated from 885 AFLP fragments.
eri Mez and P. casmichensis L.B.Sm. In ‘Yellow Puya’,
P. boliviensis Baker is sister to P. chilensis Molina and
P. gilmartiniae G.S.Varad. & A.R.Flores, which form a
monophyletic clade (PP 100). The other poorly supported (PP 73) subclade of Central & Northern Andes
places P. raimondii Harms and P. parviflora L.B.Sm
stepwise as sister to all taxa from the Northern Andes
(PP 96). Phylogenetic support is high (PP 100) for the
clade comprising Costa Rican P. dasylirioides Standl.
and species from the Eastern Cordillera of Colombia:
P. goudotiana Mez, P. trianae Baker, P. nitida Mez,
P. santosii Cuatrec., P. lineata Mez and P. bicolor Mez.
Support is lower (PP 68) for the sister clade of pri-
marily Ecuadorian species from the Western and
Central Colombia Cordilleras found in similar higher
and lower elevation habitats. Puya parviflora L.B.Sm.
and P. cajasensis Manzan. & W.Till from Ecuador are
not part of this monophyletic Ecuadorian clade, but
the positions of these taxa lack support. In the Ecuadorian clade, relationships between species from mid
elevations (e.g. P. tillii Manzan., P. roseana L.B.Sm.,
P. retrorsa Gilmartin) are poorly defined, in contrast
to a well-supported (PP 100) lineage of high-elevation
taxa (P. hamata L.B.Sm., P. maculata L.B.Sm.,
P. compacta L.B.Sm., P. pygmaea L.B.Sm. and
P. cuevae Manzan. & W.Till).
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
I
H
> 3000m
Northern
1500->3000m
Central
1500-3000m
Central
& Southern
<1500-3000m
Southern
<1500m
G
G
G
Widespread
FG
G
G
FG
G
FG
G
DG
FG
D
D
*
D
AB
A
B
BE
E
CD
D
D
C
D
C*
CD
C
D
D
D
D
E
*
A
Core
Puya
Central &
Southern Andes
D
D*
Central &
Northern Andes
Central
& Northern
P. dasylirioides
P. dasylirioides
P. santosii1*
P. goudotiana*
P. goudotiana*
P. nitida 2
P. nitida 3
P. santosii2*
P. bicolor
P. lineata
P. trianae1
P. trianae2
P. cajasensis
P. nutans
P. cuevae*
P. hamata2*
P. maculata*
Northern
P. compacta
P. pygmaea1*
Andes
P. pygmaea2*
P. hamata1*
P. navarroana
P. thomasiana
P. hirtzii
P. asplundii
P. sodiroana
P. retrorsa
P. tillii
P. roseana
P. joergensenii
P. exigua
P. nitida3
P. eryngioides
P. aequatorialis
P. obconica
P. parviflora
P.raimondii1**
P.raimondii2**
P. yakespala
P. herrerae
P. chilensis1
P. chilensis2
P. chilensis3
Yellow
P. chilensis4
P. gilmartinii
Puya
P. boliviensis 1
P. boliviensis 2
P. casmichensis
P. weberbaueri
P. angusta1
P. angusta2
P. atra
P. assurgens
P. novarae
P. claudiae
P. tuberosa
P. vallo-grandensis
P. vasquezii
P. laxa
P. stenothrysa
P. nana
P. dyckioides 1
P. pearcei
P. sanctae-crucis
P. harmsii
P. castellanosii
P. spathacea
P. dyckioides 2
P. micrantha
P. lilloi
P. olivacea
P. mirabilis 1
P. mirabilis 2
P. ultima
P. densiflora
P. sp. nov.RSJ 221
P. roezlii
P. sp.nov.RSJ 219
P. wrightii
P. lanata
P. ferreyrae
P. macrura
P. ferruginea 1
P. ferruginea 2
ZygoP. ferruginea 4
P. ferruginea 3
P. mima
morphic
P. venusta1
P. venusta2
P. venusta3
P. coerulea var. coerulea3
P. coerulea var. coerulea2
P. coerulea var. coerulea1
P. coerulea var. violacea4
P. alpestris 1
P. berteroniana
P. alpestris 3
P. alpestris 2
211
Blue
Puya
Figure 5. Priority rule consensus phylogeny of Puya. Branch thickness corresponds to phylogenetic support: thickest
lines represent posterior probability (PP) of 80 and above, medium lines represent PP of 60–79 and thin represent less
than 60 PP. Life-history types are denoted as **semelparous, *semi-semelparous. Coloured boxes next to terminal names
and pie charts above and below branches represent latitude and elevational zones. Pie charts represent the ancestral
latitudinal and elevational zones as percentages of probability determined in BayesTraits. Letters at nodes correspond to
ancestral area cordillera (sensu Simpson, 1975) as determined in S-DIVA. A, Coastal; B, Principal; C, Pampean; D,
Oriental; E, Occidental; F, Western Cordillera of Colombia; G, Central Cordillera of Colombia; H, Eastern Cordillera of
Colombia; I, Cordillera Talamanca of Costa Rica. An asterisk at nodes indicates widespread ancestor (more than two
ancestral areas). For clarity, pie charts and ancestral areas were not placed tip-ward if all resultant clades from a node
had the same value.
The backbone of the second major clade, Central &
Southern Andes, is generally less resolved, but strong
support is found for several smaller clades. A clade of
species with simple inflorescences from the Cordillera
Occidental of the central Andes (P. macrura Mez,
P. ferreyrae L.B.Sm., P. lanata Schult.f and P. wrightii
L.B.Sm.) is well supported (PP 93) as sister to the
remaining Central & Southern Andes clade. Several
undescribed taxa from Apurimac, Peru, were placed
in a clade with P. roezlii E.Morren and P. densiflora
Harms. Well-supported subclades tend to include
species found in close geographical proximity (e.g.
P. harmsii A.Cast., P. castellanosii L.B.Sm., P. spathacea Mez, P. lilloi A.Cast. and P.micrantha Mez from
the Pampean range of north-western Argentina;
P. claudiae Ibisch, R.Vásquez & E.Gross, P. tuberosa
Mez, P. vallo-grandensis Rauh, P. vasquezii Ibisch &
E.Gross, P. laxa L.B.Sm., P. stenothrysa Mez and
P. nana Wittm. from the Cordillera Oriental of central
Bolivia).
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
212
R. S. JABAILY and K. J. SYTSMA
Table 1. Parsimony reconstruction of the distribution of
Puya spp. coded as different discrete characters
Characters coded
Treesteps
Consistency
index
Retention
index
Andean Cordilleras
Latitude (two-state)
Elevation (two-state)
Latitude (three-state)
Elevation (three-state)
19
1
14
8
16
0.368
1.000
0.071
0.250
0.125
0.810
1.000
0.567
0.891
0.661
ANCESTRAL
STATE RECONSTRUCTION OF
BIOGEOGRAPHICAL CHARACTERS
Dispersal/vicariance analysis (Fig. 5) recovered the
Cordillera Oriental as the ancestral area for the
deepest ancestral nodes in the Andes. Multiple dispersals into the Cordillera Occidental and the
Pampean Ranges were found. Puya ferruginea and
P. boliviensis independently dispersed into the Cordillera Principal and Atacama Desert region. All
analyses determined a single dispersal event across
the Western Andean Portal into the Northern Andes,
with no subsequent transitions back south. Subsequently, taxa in the Eastern Cordillera of Colombia
were segregated from those of the Western and
Central Cordilleras. Transitions between the Western
and Central Cordilleras were frequent. The Cordillera
de Talamanca of Costa Rica was colonized by the
ancestor of P. dasylirioides from within the Eastern
Cordillera.
Range shifts between elevational zones were much
more frequent and less consistent in direction than
transitions between latitudinal zones (Tables 1, 2).
Likewise, there is more uncertainty surrounding the
ancestral states (Fig. 5) and a greater magnitude of
character state transitions in general in elevation
compared with latitude (Tables 1, 2). Multiple transitions into both high- and low-elevation zones from
mid-elevational zones occur in both the Central &
Southern Andes and the Central & Northern Andes
clades. BayesDiscrete did not favour a model of correlated evolution between latitude and elevation
states over character independence (P = 0.1, c2 = 7.92,
d.f. = 4). The independent model found that evolutionary transitions between elevational zones, regardless
of latitude, were more frequent than transitions in
latitude (Fig. 6).
EVOLUTION
OF LIFE-HISTORY VARIABILITY
Field observations clarified three life-history categories within Puya (Fig. 5, Table 3). All individuals of
P. raimondii surveyed were composed of a single
rosette, and are deemed semelparous (Fig. 1C). Most
Table 2. Relative transition rates (q) of Puya spp. in latitude (1–6) and elevation (7–12) and significance of selected
hypotheses
1
2
3
4
5
6
7
8
9
10
11
12
qxz = Relative q values
Hypothesis
transition rate calculated testing
(q) from x to y from data proposals
Likelihood
ratio
test
q02
q01
q20
q10
q12
q21
q02
q01
q20
q10
q12
q21
0.076
1.315
15.416
0.066
0.076
0.0008
0.397
0.466
20.023
6.322
0.362
0.118
0.047
0.061
0.092
0.435
0.480
0.482
0.262
0.858
0.246
1.028
0.886
2.078
q02 = q20
q01 = q10
q21 = 0
q12 = q21
q20, q02 = 0
q01 = 0
q02 = q20
q01 = q10
q21 = 0
q12 = q21
q20, q02 = 0
q01 = 0
Characters are 0 = north of WAP, 1 = WAP to Tropic of
Capricorn, 2 = south of Tropic of Capricorn; 0 = < 1500 m,
1 = 1500–3000 m, 2 = > 3000 m; bold type indicates significant at P = 0.001.
north, high
north, low
south, high
south, low
Figure 6. Relative frequencies of evolutionary transitions
between latitudinal and elevational zones of Puya lineages. For latitude, ‘north’ denotes north of the Western
Andean Portal and ‘south’ denotes south of the Western
Andean Portal. For elevation, ‘low’ indicates less than
3000 m, and ‘high’ indicates 3000 m and above. Arrow
thickness is proportional to relative rate of transition
calculated under the independent model of BayesTraits
Discrete.
other Puya spp. observed in the field were found to be
iteroparous, with mature individuals composed of
multiple, attached rosettes by the age of inflorescence
production (Fig. 1D). Iteroparous species are composed of several to thousands of interconnected
rosettes by the age of sexual reproduction. An intermediate category, ‘semi-semelparous’, is used to
describe several species with attached rosette pups
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
Lax/less conspicuous
Primarily dry; often on steep
and rocky slopes
Low to high
Minimal
Ample
Densely strobiliform/
highly conspicuous
Primarily wet; often in rich,
waterlogged soil; terrain can
be flat
High
All individuals composed of a single rosette at all points in the life cycle, and never produce vegetative pup rosettes
Semelparous, e.g. Puya
raimondii
Semi-semelparous, e.g. Puya
hamata, P. goudotiana,
P. clava-herculis, P. santosii,
P. pygmaea
Iteroparous, e.g. Puya trianae,
P. chilensis, P. dyckioides,
P. ferruginea
213
occurring in only a subset of reproductive-aged individuals in a population. Exemplar semi-semelparous
species P. goudotiana, P. santosii and P. hamata are
all relatively tall (1.5–c. 3.0 m including the inflorescence) and found commonly in high-elevation wet
páramo habitats in Colombia and Ecuador.
BayesMultistate recovered the ancestral lifehistory state of Puya as iteroparous with 90% probability. Semelparous P. raimondii is placed as sister
to a clade containing all of the sampled semisemelparous taxa and many iteroparous taxa from
the northern Andes (Fig. 5). In the northern Andean
clade, semi-semelparity apparently evolved independently several times.
DISCUSSION
AFLP data were employed to produce a well-resolved
expanded phylogenetic tree for Puya that corroborates and enhances the emerging picture of evolution
of the genus from nuclear and plastid DNA sequences
and previous AFLP analysis (Jabaily & Sytsma, 2010;
Schulte et al., 2010; Givnish et al., 2011). Despite lack
of resolution due to low sequence variation in Andean
‘Core Puya’, Jabaily & Sytsma (2010) found some
evidence for major clades corresponding to broad geographical areas. The results presented here offer an
even more detailed but similar picture in terms of
broad geographical structure across the phylogeny.
THE
ROLE OF HYBRIDIZATION IN THE
EVOLUTION OF
Some individuals in a
population produce vegetative
pup rosettes before or after
inflorescence production but
others do not
All flowering individuals
composed of multiple
interconnected rosettes
Elevational range
Table 3. Life-history categories, example species and descriptions for Puya
Habitat description
Inflorescence
Definition
Category
Indument
density
BIOGEOGRAPHY OF PUYA
PUYA
Schulte et al. (2010) sampled extensively throughout
the distribution of the seven Chilean Puya spp. and
used AFLP data to investigate the prevalence of interspecific hybridization. Hybridization at various levels
was noted between and putatively within the phylogenetically well-defined major groups of Chilean Puya
(‘chilensis’: P. chilensis, P. gilmartiniae, P. boliviensis;
‘alpestris’: P. alpestris, P. berteroniana Mez; ‘coerulea’:
P. venusta Phil. in Baker and P. coerulea Miers and
associated varieties), particularly where species occur
in sympatry. The NeighborNet analysis presented
here resolves the same three major Chilean groups,
and suggests greater frequency of non-bifurcation
events in these groups than between other clusters of
species from elsewhere in the Andes. This could indicate that hybridization is particularly common among
the Chilean Puya spp. or could be an artefact of the
sparser taxon and within-species sampling in the
Andes compared with Chile in this study.
Reproductive isolating factors among Chilean Puya
spp. are apparently limited, in line with weak preand post-zygotic barriers across Bromeliaceae (Wendt
et al., 2001, 2008). Multiple species in the presented
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
214
R. S. JABAILY and K. J. SYTSMA
phylogeny were recovered as non-monophyletic (e.g.
P. santosii, P. dyckioides Mez), which could be indicative of a putative hybrid origin of these accessions,
incomplete lineage sorting or species delimitation
problems. Population-level sampling of widespread,
morphologically variable and/or putatively nonmonophyletic species would be necessary to investigate the extent of introgression in populations of
Puya in the Andes. In one such study, interpopulation
AFLP analysis of Puya raimondii found markedly low
levels of polymorphism and high levels of inbreeding
(Sgorbati et al., 2004), indicating that introgression
may not be ubiquitous in Puya. The nearest relatives
of most of the species included in the present study
often occur in close geographical proximity. As with
Chilean Puya (Schulte et al., 2010), geographical isolation at a local scale, such as species endemic to
different elevational zones on the same mountain
range, may be the predominant prezygotic reproductive barrier among the Andean Puya spp. In plant
communities of the páramos, e.g. in Colombia, P. goudotiana, P. trianae Baker, P. santosii and P. nitida
occur in true sympatry.
Incongruence between maternally inherited and
biparentally inherited gene trees in earlier phylogenetic analyses of Jabaily & Sytsma (2010) and morphological and ecological evidence corroborate the
study of Schulte et al. (2010) suggesting that several
ancient interspecific hybridization events were probably involved in formation of the seven extant
Chilean Puya spp., including the origin of the ‘alpestris’ group as potential homoploid hybrid species
(polyploidy is not known in Puya and is very rare in
Bromeliaceae). These events were discerned by analyzing the discordance between phylogenies derived
from maternal and biparental loci, in combination
with morphological and ecological information. Homoploid hybrid speciation is often mediated by strong
ecological selection and spatial segregation (Rieseberg
& Willis, 2007). These conditions are probably
common across elevational gradients in narrow interAndean valleys, where unique biotic communities
occur at different elevations and aspects in close
spatial proximity, and may well have been factors in
the early hybrid-mediated evolutionary events in
Puya.
HISTORICAL
BIOGEOGRAPHY SCENARIO FOR
PUYA
The Bromeliaceae-wide time-calibrated plastid DNA
phylogeny of Givnish et al. (2011) included eight Puya
spp. and estimated the divergence time of Puya from
its sister clade, Bromelioideae, at 10.1 Mya (range for
100 random trees 8.37–12.64 Mya), with the crown
radiation of extant taxa in the Andes estimated at
3.5 Mya, and in Chile at 2.5 Mya. These estimates,
based on the best available data in this rapidly evolving group with low levels of molecular evolution, place
the origin of the major clades and extant Puya spp. in
the timeframe of the final uplift of the Andes and
subsequent Pleistocene glaciation cycles. The AFLP
phylogenetic tree presented here and distribution patterns of most taxa further suggest that both late
Neogene and early Quaternary geological timeframes
and associated processes were important in shaping
the evolution of the group. The combination of ancestral state reconstructions, elevational and latitudinal
distributions, and the expanded phylogeny of Puya
provide four key pieces of evidence about the evolutionary history of Puya: (1) the monophyletic northern
Andean lineage is derived from within a broad central
Andean clade, with no transitions back across the
Western Andean Portal; (2) subsequent cladogenesis
between adjacent cordilleras and different elevational
zones were common and multidirectional; (3) the
number of Puya spp. increases towards the equator,
but fewer Puya spp. are found at and especially north
of the equator; and (4) the greatest number of species
and most narrow endemics are found at midelevations, above the moist forest and below the highelevation habitats.
These results suggest that Puya originated in
central Chile, where many early branching lineages of
the sister subfamily Bromelioideae are also endemic,
along with the Chilean clade that is sister to the rest
of the primarily Andean ‘Core Puya’ clade. Early
divergence of the major clades of Bromelioideae and
the two major clades of Puya is indicated by the short
branch lengths in the analyses of Givnish et al. (2011)
and Jabaily & Sytsma (2010). Species from south of
the Tropic of Capricorn including Puya of Chile and
the lowlands of Argentina generally have much
broader elevational and latitudinal ranges than those
from tropical latitudes, with the number of narrow
endemics generally increasing north towards the
equator (Fig. 2). Temperate latitudes and associated
high seasonality may also represent the limits of
the climatic niche for Puya, with few species known
from higher elevations at temperate latitudes in the
Andes. However, newly discovered species from highelevation habitats in western Argentina indicate that
further fieldwork is needed to establish the range
limits of the genus with greater certainty (Aráoz &
Grau, 2008; Gómez Romero & Grau, 2009).
The Andean orogeny proceeded generally from
south to north and the broad biogeographical pattern
of Puya cladogenesis, also from south to north, also
reflects this overall progression of Andean uplift. The
movement of Puya into the Cordillera Oriental,
whether via dispersal as suggested by S-DIVA or via
the vicariant process of mountain uplift, effectively
segregated the Chilean lineage of Puya from the
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BIOGEOGRAPHY OF PUYA
Andean (before the later secondary reintroduction of
the ‘Yellow Puya’ lineage back into Chile, as discussed
by Jabaily & Sytsma, 2010). Major mountain uplift
events were punctuated by long periods of relative
stability, with the various cordilleras at half the
average and maximum height between 23 and 11 Mya
and an additional uplift of over 2000 m occurring
later in the Quaternary (Graham, 2010). Common
vegetation types in the emerging Andes prior to the
late Miocene include lowland rainforest and montane
broadleaved forest (Graham, 2010), which today are
generally devoid of Puya, a lineage generally intolerant of extensive shading. Seasonally dry tropical
forests have been present since before the putative
time of the Puya crown radiation (Pennington et al.,
2010; Särkinen et al., 2011) and today many Puya
spp. of mid to lower elevations are endemic to
steep valleys where these forests dominate and rocky
outcrops are common. Thus, suitable dry habitats
lacking dense tree cover may have been present for
Puya spp. to invade the Andes, with extensive cladogenesis hypothesized to have occurred in the Cordillera Oriental before Puya moved into adjacent ranges
to the north.
Puya apparently traversed the WAP zone from the
central Andes only once, with no subsequent transitions back south. The WAP presented a potentially
important barrier to many groups of organisms (Vuilleumier, 1969; Duellman, 1979; Ayers, 1999; Andersson, 2006; Antonelli et al., 2009; Cosacov et al., 2009)
and is an area exhibiting high endemism for many
other groups (Berry, 1982; Weigend, 2002; Smith &
Baum, 2006). The inland incursion of the ocean at the
WAP receded with the uplift of the Andes, and was
gone by the mid-Miocene, suggesting a dispersal
rather than vicariant explanation for the distribution
of extant Puya, given current divergence time estimates for the group. The WAP region today houses a
large number of narrowly endemic Puya spp., both to
the north and to the south, with just two widespread
species (P. hamata, P. lanata) present on both sides,
presumably the results of subsequent dispersal
events across the WAP.
The northern Andes (particularly Colombia and
Venezuela) generally have fewer Puya spp. than
similar habitats in the central Andes, perhaps indicative of the relatively recent colonization of these
younger parts of the Andes or the smaller physical
area of high-elevation or dry inter-Andean habitats
suitable for Puya compared with the more extensive
Cordilleras Occidental and Oriental south of the
WAP. One of the most prominent patterns in global
biogeography is increased species richness towards
the equator (Wiens & Donoghue, 2004; Weir, 2006;
Mittelbach et al., 2007). The number of Puya spp.
increases roughly linearly from temperate latitudes
215
towards the equator, but fewer Puya spp. are found at
and especially north of the equator than would be
predicted by a linear model. The actual latitudinal
zone with the greatest number of species is not at the
equator, but is rather from central Peru into central
Bolivia, where most species are found in inter-Andean
valleys. This region with highest diversity of Puya is
also the same for Andean Solanum L. (Knapp, 2002).
The northernmost Puya lineages are thus postulated
to be some of the most recently derived.
The evolutionary progression of Puya along the
Andes was most probably primarily, but not unidirectionally, from south to north. The lower-elevation
Pampean region of Argentina was colonized multiple
times from neighbouring regions of the Cordillera
Oriental. Once these central Andean derived lineages
moved into lower elevations on the eastern slope of
the Andes, there were no subsequent transitions in
elevation or latitude, with the probable caveat that
the recently discovered high-elevation taxa (Gómez
Romero & Grau, 2009) were not sampled. This may
suggest that these are also more recently colonized
areas, or alternatively that these lowland chaco habitats mark the ecological limits of where the lineage
can live.
ALLOPATRIC SPECIATION DRIVEN BY
PLEISTOCENE GLACIAL CYCLES
The apparently frequent evolutionary transitions of
Puya both up and down in elevation, indicated today
by the occurrences of closely related species at different elevations in the same latitudinal zone, and frequent transitions between adjacent cordilleras (e.g.
Western and Central Colombian Cordilleras, Fig. 5)
provide possible evidence for speciation via a glacial
‘pump’ during the Pleistocene. Once the major lineages of Puya were in place throughout the central and
northern Andes, glacially driven cyclical fragmentation of populations could have been a driver of allopatric speciation in Puya. Multiple glacial cycles in
the tropical Andes occurred during the Pleistocene,
causing tropical and montane forests to move down by
as much as 1200–1500 m during glacial maxima and
move up in elevation during interglacial periods (van
der Hammen, 1974). Cooler ecosystems such as the
puna and páramo are postulated to have expanded
and contracted (Haffer & Prance, 2001). Puya spp.
have relatively poor seed dispersal capabilities and
relatively long life spans (Benzing, 2000), suggesting
that populations may not have been as mobile to
track a given climate envelope during the Pleistocene
glacial cycles. If populations were subsequently isolated, adaptation to the regional temperature and
moisture regimes of the valley or mountain range
where the lineages remained may have followed,
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
216
R. S. JABAILY and K. J. SYTSMA
leading to allopatric speciation. Puya is the only bromeliad genus to have evolved CAM photosynthesis
multiple times (Martin, 1994; Benzing, 2000; Crayn,
Winter & Smith, 2004; Givnish et al., 2007) and thus
was adapted to a wide variety of both xeric and mesic
habitats in the Neotropics. A more precisely scaled
molecular dated phylogeny of the group beyond that
of Givnish et al. (2011) would be crucial to testing the
putative timing suggested by this scenario, as the
crown diversification of many species-rich South
American plants and animals has been determined to
have occurred prior to the onset of Pleistocene glaciation cycles (Hoorn et al., 2010).
The greatest number of species in Puya is found at
mid elevations (2600–3300 m) in the central Andes.
This mid-elevational species diversity ‘hump’ fits with
broader global trends in species richness with elevation (Rahbek, 1995; Kluge, Kessler & Dunn, 2006;
Lomolino, Riddle & Brown, 2006). Colwell & Hurtt
(1994) postulated that mid-elevations should have the
highest species richness in a given group because
these elevations are the maximum distance from the
‘hard boundaries’ imposed by elevation-dependent
environmental factors at both the upper and the
lower limits for a group of organisms. A lower elevational boundary for most Puya may be the dominance
of various kinds of Neotropical forest, particularly on
the eastern slope of the Andes as lower elevation
species are frequent along the western slope in seasonally dry valleys and matorral habitats. At the
upper elevational boundary, the diurnally harsh highelevation páramo and puna habitats present unique
challenges that only a limited number of Puya lineages have been able to overcome. Expansion of ecological niche modelling to Andean Puya (currently
only available for Chilean taxa; Zizka et al., 2009)
would allow for more explicit identification of ecological factors that shape current distributional patterns
and more detailed biogeographical scenarios to be
hypothesized (Nakazato, Warren & Moyle, 2010).
Many groups of Andean organisms show similar
phylogenetic and biogeographical patterns to Puya
and evolved in the same late Cenozoic time period.
Major systematic divisions in Andean groups often
correspond to major latitudinal divisions (e.g. northern Andes/central Andes; Ezcurra, 2002; Smith &
Baum, 2006; Amico, Vidal-Russell & Nickrent, 2007).
More recently diverged species are often found in the
geologically younger northern Andean cordilleras and
older lineages are found further south, corresponding
to the south-to-north pattern of Andean uplift (Moritz
et al., 2000; Emshwiller, 2002; Torres-Carvajal, 2007;
Soejima et al., 2008; Cosacov et al., 2009; Simpson
et al., 2009). Widespread lowland taxa have given rise
repeatedly to localized, high-elevation groups
(Simpson, 1979; Emshwiller, 2002; Hall, 2005; Fjeldsa
& Rahbek, 2006; Brumfield & Edwards, 2007; Ribas
et al., 2007; Bonaccorso, 2009), although in some
cases mid to high elevations can be the source for
lowland taxa (Elias et al., 2009). Uplift of the Andes
and subsequent climate change, whether increased
aridity or shifting vegetation belts in response to
glaciation, were major events in Heliotropium L.
(Luebert et al., 2011), Chuquiraga Juss. (Ezcurra,
2002), Lepechinia Willd. (Drew & Sytsma, 2012) and
many others.
LIFE-HISTORY
CLASSIFICATION IN
PUYA
Field observations corroborate clear differences in the
production of vegetative (‘pup’) rosettes among Puya
spp. (most species do, and few species do not) and this
life-history trait is apparently fixed within species.
The majority of species are iteroparous, readily producing pups before and after production of inflorescences. Although each individual rosette produces
a single terminal inflorescence (hapaxanthic), sympodially branched hapaxanthic plants are considered
to be iteroparous (Young & Auspurger, 1991; Benzing,
2000). Iteroparous Puya spp. grow in the coastal
matorral of central Chile, steep cliff-faces of
inter-Andean valleys and in sympatry with semisemelparous and semelparous species in highelevation páramo and puna habitats (Fig. 1A).
Individuals within a species can vary greatly in the
number of rosettes that make up their body at reproductive age and in overall plant size (Augspurger,
1985) and iteroparous species differ greatly in habitat
and broad morphology, including inflorescence types
(simple, compound, strobiliform etc.).
Non-iteroparous species are few, with only P. raimondii from the high-elevation puna of Bolivia and
Peru being apparently entirely semelparous. Individuals appear not to produce pup rosettes before or
after production of the terminal inflorescence and
total senescence follows seed dispersal (Fig. 5C).
Semi-semelparous species from high-elevation
páramo habitats have a similar, but not as extreme,
life history (e.g. P. hamata and P. goudotiana) with
some, but not all, individuals producing pup rosettes
before and/or after production of the terminal inflorescence; clonal individuals are generally composed of
many fewer rosettes than related iteroparous species.
The current phylogenetic analysis suggests that noniteroparity has evolved multiple times, with no apparent trend of semi-semelparity as an intermediate step
leading to true semelparity. More complete taxon
sampling, including P. weberiana E.Morren ex Mez
and P. bravoi Aráoz & A.Grau, recently identified as
monocarpic in the new treatment of Puya in Argentina (Gómez Romero & Grau, 2009), is needed to
provide new insight into the evolution of this curious
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
life-history strategy. Similarity in overall morphology
and habitat preferences amongst non-iteroparous
Puya spp. suggests that life-history type may be predicted for other taxa (Table 3).
Semelparity has convergently evolved in many
long-lived, rosette-forming taxa from tropical
montane ecosystems, including several Hawaiian
Argyroxiphium DC (Robichaux et al., 1990), Ruilopezia Cuatrec. (Cuatrecasas, 1968), some species of
Espeletia Nutt. (Berry & Calvo, 1989) and Lobelia
telekii Schweinf. ex Engl. from east Africa (Young,
1984). The repeated derivation of non-iteroparity in
Puya is similar to patterns observed within Aeonium
Webb & Berthel. (Jorgensen & Olesen, 2001), but
differs from the single derivation in Agave L. (GoodAvila et al., 2006) and island-dwelling Echium L.
(Böhle, Hilger & Martin, 1996). Non-iteroparity is
relatively rare in Puya, as it is in Yucca L. (Schaffer
& Schaffer, 1977; Huxman & Loik, 1997), and may
represent a more local adaptation to harsh conditions in high-elevation habitats, rather than a key
innovation prompting diversification, as found for
monocarpy in the genera Agave and Furcraea Vent.
(Good-Avila et al., 2006).
Puya raimondii is one of the most striking and
well-studied species of Puya (Sgorbati et al., 2004) and
one of the most wide-ranging species latitudinally, but
is restricted to high-elevation puna habitats. Importantly, it is the largest and most likely the longest lived
bromeliad species, with heights to > 12 m and age
estimates of flowering individuals of 60–100 years
(Hartman, 1981; Hornung-Leoni & Sosa, 2004). Semisemelparous high-elevation P. hamata and P. goudotiana from the northern Andes páramos are the next
tallest Puya spp. and can reach heights of > 5 m, taking
many decades to reach maturity (Smith & Downs,
1974; Manzanares, 2005). Delayed reproduction, slow
growth and massive inflorescences are the hallmarks
of semelparity in long-lived rosette plants, which incur
trade-offs between increased resource allocation in
current fecundity at the expensive of future, subsequent fecundity (Young & Auspurger, 1991).
Evolution of semelparous life history has been
explained by two different models: (1) the reproductive effort model and (2) the demographic model. The
reproductive effort or ‘big bang’ model of evolution
of semelparity predicts that increasing rewards of
greater fecundity for each additional investment
of resources in reproduction will drive the evolution of
semelparity (Schaffer & Schaffer, 1977). For example,
if the number of pollinators is relatively low compared
with the number of flowers, pollinators may select
for larger floral displays to optimize foraging. For
semelparous P. raimondii, the sheer size of the inflorescence, often with > 100 000 flowers and copious
nectar, attracts many species of hummingbirds and
217
passerine birds (Hornung-Leoni, Sosa & Lopez, 2007)
lending anecdotal support to this theory, as do the
relatively large size of semi-semelparous P. hamata
and P. goudotiana inflorescences. In many other
plant groups, larger inflorescences and a significantly
shorter post-flowering half-life are found in semelparous species than in closely related iteroparous
species (Young, 1984; Rocha, Valera & Eguiarte,
2005).
The demographic or bet-hedging model (reviewed
by Young, 1990) predicts that semelparity should be
favoured in habitats where climates are harsh and
future reproduction is less likely or infrequent. In
other plant groups, including the giant bromeliad
Alcantarea Harms (Barbará et al., 2009), iteroparous
species are found primarily at low to mid elevations,
and semelparous species are found in more arid or
harsh high elevations (Young, 1984; Good-Avila
et al., 2006). In support of this model in Puya, all
non-iteroparous species are restricted to high elevations in the Andes in habitats that experience strong
diurnal temperature fluctuations, ice crystal formation, solifluction and intense solar radiation (Balslev
& Luteyn, 1992), factors that limit seedling establishment. Miller & Silander (1991) reported that
seedlings of ‘monocarpic’ P. clava-herculis Mex &
Sodiro in the Ecuadorian páramos almost exclusively
establish next to grass tussocks that protect the
seedling from the elements and help to prevent
solifluction.
Other giant rosette plants of high-elevation tropical
montane ecosystems branch less frequently and in
turn produce a greater number of leaves per rosette
that serve to insulate the meristem from freezing
nocturnal temperatures (Monasterio, 1986). The
rosettes of P. raimondii and other non-iteroparous
taxa appear to be composed of a much greater number
of leaves than iteroparous relatives (Fig. 1), which
may serve to insulate the meristem. The leaves of
high-elevation Puya are typically glabrous or only
sparsely pubescent, with more direct insulation from
the dense lanate hairs that cover the inflorescence
axes, bracts and sepals (Fig. 1B) providing more
direct insulation to regulate the temperature of the
ovaries and promote seed set (Miller, 1986). Numerous leaves may also be beneficial during fires because
marcescent leaves at the rosette base protect the
meristem from fire, and also serve to elevate the
apical meristem higher above the ground (Givnish,
McDiarmid & Buck, 1986). As with Espeletia in the
northern Andes (Cuatrecasas, 1968), mature P. raimondii rosettes with blackened lower leaves are commonly seen in the high puna, although human-caused
fires of the inflorescence are a major conservation
concern (Hornung-Leoni & Sosa, 2004; Sgorbati et al.,
2004).
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
218
R. S. JABAILY and K. J. SYTSMA
FUTURE
AREAS OF RESEARCH
Phylogenetic analysis of many Andean plant groups is
rapidly progressing, allowing for broad patterns
across the massive geographical space and geological
time to be deciphered. With next-generation sequencing methodologies becoming more commonplace in
species-level systematics (Egan, Schlueter & Spooner,
2012; Fay, 2012), well-resolved and robustly supported phylogenetic trees will become available for
species-rich high-elevation Andean clades such as
Puya. The next iteration of phylogenetic analysis in
Puya will need to be based on larger DNA sequence
data sets and should target additional species from
high-elevation habitats with different life histories.
This will allow for rigorous time-calibration of the
Puya phylogeny using modern molecular dating
approaches (which are currently nascent for AFLP
datasets; Kropf et al., 2009) and enable the incorporation of Puya into meta-analyses of the biota of the
Andes (Hoorn et al., 2010; Antonelli & Sanmartín,
2011; Rull, 2011; Särkinen et al., 2011; Sklenář et al.,
2011), further enhancing our understanding of the
importance of geological events in the Cenozoic.
Denser taxon sampling is needed to corroborate the
emerging historical biogeographical narrative.
More extensive field and herbarium data are also
needed to fully develop these ideas in a comparative
phylogenetic framework. Precise species distributions
are often not known for Andean plant taxa because of
the paucity of collections from many remote locations
and difficulties with species delimitation in evolutionary young lineages. Puya is certainly not without these
issues, and the distribution patterns discussed here
reflect the current incomplete state of collecting efforts
and taxonomy in the various Andean regions (Betancur & Callejas, 1997; Manzanares, 2005; Gómez
Romero & Grau, 2009; Cano Flores & Jabaily, 2010).
Many collectors of Puya specimens (including types)
did not record information on key life-history traits,
which cannot be scored from the specimens themselves. Furthermore, life-history traits were not
recorded for the vast majority of Puya species descriptions or ecological observations with the notable
exception of Monasterio (1980), Laegaard (1992),
Manzanares (2005) and Gómez Romero & Grau
(2009). Beyond P. raimondii, however, caution is
urged in assigning other Puya to the semelparous or
monocarpic life-history category. Additional field
observations, ecological data and detailed demographic surveys of populations for species with differing life-history strategies are needed, particularly in
high-elevation Andean habitats. Hopefully, these
efforts will encourage careful observation and further
studies of life history in the field in the primarily
Neotropical Bromeliaceae and other groups.
Beyond assessing taxonomic strategies and determining biogeographical history, phylogenies of
Andean taxa should be used as a framework in which
to develop and test evolutionary hypotheses. For
example, pinpointing the exact relationship between
iteroparous and non-iteroparous Puya spp. living in
sympatry in northern Andean páramos would help
shape an evolutionary ecological study of the energetic trade-offs in life-history evolution. This phylogenetic information would be coupled with intensive
demographic surveys of the populations, as the bethedging model predicts that the demography of low
adult survivorship, long periods between reproductive
events and early senescence would tend to evolve
semelparity. Multi-year demographic information is
only available for Puya dasylirioides of Costa Rica
(Augspurger, 1985) and much more long-term population monitoring effort should be expanded to other
species.
Additional field studies of life-history evolution in
the Equatorial Andes are a high priority for future
work because of the potential implication for conservation. The long life spans and reliance upon seed
production for perpetuation make non-iteroparous
taxa specifically vulnerable to grazing, fire and
climate change pressures, predicted to increase in
tropical alpine habitats (Balslev & Luteyn, 1992; Williams, Jackson & Kutzbach, 2007). The revision of
Manzanares (2005) is notable for considering lifehistory status when assigning IUCN conservation
status to Ecuadorian Puya. When choosing what to
prioritize for study in a mega-diverse area such as the
tropical Andes, taxa at greatest risk for extinction
because of their distribution or evolutionary history
should be given immediate attention.
ACKNOWLEDGEMENTS
We thank C. Williams, M. Jabaily, R. Vásquez,
E. Narváez, J. Manzanares, D. Gutierrez, W. Till,
L. Novara, M. Rosas, D. Stanton, M. Diazgranados,
J. Vanegas, D. Rodrigeuz, J. Crisci, L. Katinas,
N. Anaya, A. Tupayacha, M. Nuñez, F. Pelaéz,
W. Galiano Sanches, M. Ames, B. Drew, A. Cano,
N. Cano, N. Sevillano, M. Fernandez, K. Peterson,
S. Friedrich, E. Williams, T. Theim and G. Lyons and
the Huntington Botanical Garden. Portions of this
research were made possible with funding support
from the Cactus and Succulent Society, Mayers Fellowship at the Huntington Institute, Bromeliad
Society International Research Grant, Garden Club of
America, American Society of Plant Taxonomists,
Cuatrecasas Travel Award (US) and the National
Science Foundation Graduate Research Fellowship
programme.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
BIOGEOGRAPHY OF PUYA
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APPENDIX 1
Voucher information and localities for specimens used
in AFLP analysis.
Puya aequatorialis André, RSJ 097 (QCNE) Ibarra,
Ecuador. Puya alpestris Poepp., 1. RSJ 007 (WIS)
Huntington Bot. Gar. USA; 2. RSJ 177 (WIS) Constitution, Chile; 3. RSJ 174 (WIS) Curacavi, Chile. Puya
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angusta L.B.Sm., 1. RSJ 226 (WIS) Ancash, Peru; 2.
RSJ 230 (WIS) Ancash, Peru. Puya asplundii
L.B.Sm., RSJ 098 (QCNE) Cotacachi, Ecuador. Puya
assurgens L.B.Sm., RSJ 026 (WIS) Huntington Bot.
Gar., USA. Puya atra L.B.Sm., RSJ 974 (WIS)
Comarapa, Bolivia. Puya berteroniana Mez, RSJ
168 (WIS) Fray Jorge, Chile. Puya bicolor Mez, RSJ
202 (COL) Villa de Leyva, Colombia. Puya boliviensis Baker 1. M. Rosas s.n. (WIS) Chile; 2. D. Stanton
s.n. (WIS) Chile. Puya cajasensis Manzan. & Till,
RSJ 128 (QCNE) Cajas, Ecuador. Puya casmichensis L.B.Sm., RSJ 223 (WIS) Otuzco, Peru. Puya castellanosii L.B.Sm., RSJ 148 (WIS) Lago Brealito,
Argentina. Puya chilensis Molina, 1. RSJ 164 (WIS)
Zapallar, Chile; 2. RSJ 171 (WIS) La Serena, Chile; 3.
RSJ 172 (WIS) Mineral de Talca, Chile; 4. RSJ 170
(WIS) Totoralillo, Chile. Puya claudiae Ibisch,
Vásquez & E. Gross, RSJ 065 (WIS) Samaipata,
Bolivia. Puya coerulea var. coerulea Miers, RSJ
085 (WIS) Huntington Bot. Gard., USA; 2. RSJ 175
(WIS) Cauquenes, Chile; 3. RSJ 176 (WIS) Constitution, Chile. var. violacea, 4. RSJ 057 (WIS) Huntington Bot. Gard, USA. Puya compacta L.B.Sm.,
RSJ 129 (QCNE) Cajas, Ecuador. Puya cuevae
Manzan. & Till, RSJ 110 (QCNE) Cerro Toledo,
Ecuador. Puya dasylirioides Standl. F 2141915; B.
Berger s.n. (WIS) Cerro de la Muerte, Costa Rica.
Puya densiflora Harms, RSJ 213 (WIS) Cusco, Peru.
Puya dyckioides Mez, 1. RSJ 067 (WIS) Samaipata,
Bolivia; 2. RSJ 150 (WIS) Salta, Argentina. Puya
eryngioides André, RSJ 114 (QCNE) Podocarpus,
Ecuador. Puya exigua Mez, RSJ 134 (QCNE)
Matanga, Ecuador. Puya ferreyrae L.B.Sm., RSJ 222
(WIS) Trujillo, Peru. Puya ferruginea (Ruiz & Pav.)
L.B.Sm., 1. RSJ 059 (WIS) Huntington Bot. Gard.; 2.
RSJ 209 (WIS) C’orao, Peru; 3. RSJ 210 (WIS) Pisac,
Peru; 4. RSJ 214 (WIS) Tres Cruces, Peru; Puya
gilmartiniae G.S.Varad. & A.R.Flores. Puya goudotiana Mez, RSJ 182 (COL) Cruz Verde, Colombia;
RSJ 207 (COL), Colombia. Puya hamata L.B.Sm., 1.
RSJ 090 (QCNE) El Angel, Ecuador; 2. RSJ 122
(QCNE) Fierro Urcu, Ecuador. Puya harmsii
(A.Cast.)A.Cast., RSJ 145 (WIS) Tafi del Valle, Argentina. Puya herrerae Harms, RSJ 212 (WIS) Urubamba, Peru. Puya hirtzii Manzan. & Till, RSJ 096
(WIS) Buenos Aires, Ecuador. Puya lanata Schult.,
RSJ 105 (QCNE) Catamayo, Ecuador. Puya laxa
L.B.Sm., RSJ 190 (WIS) Comarapa, Bolivia. Puya
lilloi A.Cast., Till B134 (WU). Puya lineata Mez,
RSJ 180 (COL) Cruz Verde, Colombia. Puya
macrura Mez, RSJ 230 (WIS) Caraz, Peru. Puya
maculata L.B.Sm., RSJ 120 (QCNE) Fierro Urcu,
Ecuador. Puya micrantha Mez, RSJ 151 (WIS),
Salta, Argentina. Puya mima L.B.Sm. & Read, RSJ
228 (WIS) Caraz, Peru. Puya mirabilis (Mez)
L.B.Sm., 1. RSJ 153 (WIS) Salta, Argentina; 2. RSJ
161 (WIS) La Candelaria, Argentina. Puya nana
Wittm., RSJ 062 (WIS) El Fuerte, Bolivia. Puya navarroana Manzan. & Till, RSJ 137 (QCNE) Matanga,
Ecuador. Puya nitida Mez, 1. RSJ 112 (QCNE) Podocarpus, Ecuador; 2. RSJ 179 (COL) Tablaso, Colombia; 3. RSJ 206 (COL) Chingaza, Colombia. Puya
novarae G.S.Varad. ex Gómez Rom. & A. Grau, RSJ
156 (WIS) Santa Victoria, Argentina. Puya nutans
L.B.Sm., RSJ 133 (QCNE) Matanga, Ecuador. Puya
obconica L.B.Sm., RSJ 106 (QCNE) Cerro Toledo,
Ecuador. Puya olivacea Wittm., RSJ 068 (WIS) El
Portal, Bolivia. Puya parviflora L.B.Sm., RSJ 103
(WIS) Catamayo, Ecuador. Puya pearcei Mez, RSJ
038 (WIS) Huntington Bot. Gard., USA. Puya
pygmaea L.B.Sm., 1. RSJ 121 (QCNE) Fierro Urcu,
Ecuador; 2. RSJ 135 (QCNE) Matanga, Ecuador.
Puya raimondii Harms, 1. RSJ 048 (WIS) Huntington Bot. Gar. USA; 2. RSJ 230 (WIS) Ancash, Peru.
Puya roezlii E.Morr., RSJ 220 (WIS) Abancay, Peru.
Puya roseana L.B.Sm., RSJ 115 (QCNE) Saraguro,
Ecuador. Puya sanctae-crucis (Baker)L.B.Sm., RSJ
060 (WIS) Santa Cruz, Bolivia. Puya santosii
Cuatrec., 1. RSJ 186 (COL) Laguna Verde, Colombia;
2. RSJ 194 (COL), Colombia. Puya sodiroana Mez,
RSJ 100 (QCNE) Calacali, Ecuador. Puya sp. nov.,
RSJ 221 (WIS) Abancay, Peru. Puya sp. nov., RSJ
219 (WIS) Cunyac, Peru. Puya spathacea Mez, RSJ
163 (WIS) Cordoba, Argentina. Puya stenothyrsa
Mez, RSJ 073 (WIS) Comarapa, Bolivia. Puya thomasiana André, RSJ 104 (QCNE) Catamayo,
Ecuador. Puya tillii Manzan., RSJ 143 (QCNE)
Tandapi, Ecuador. Puya trianae Baker, 1. RSJ 183
(COL) Laguna Verde, Colombia; 2. RSJ 192 (COL)
Villa de Leyva, Colombia. Puya tuberosa Mez, RSJ
063 (WIS) El Fuerte, Bolivia. Puya ultima L.B.Sm.,
RSJ 051 (WIS) Huntington Bot. Gard., USA. Puya
vallo-grandensis Rauh. RSJ 070 (WIS) Vallegrande,
Bolivia. Puya vasquezii Ibisch & Gross R. Vasquez
s.n. (USZ). Puya venusta Phil., 1. RSJ 006 (WIS),
Huntington Bot. Gard., USA; 2. RSJ 165 (WIS) Valparaiso, Chile; 3. RSJ 166 (WIS) Coquimbo, Chile.
Puya weberbaueri Mez, RSJ 217 (WIS) Aguas
Calientes, Peru. Puya wrightii L.B.Sm., RSJ 039
(WIS). Huntington Bot. Gard., USA. Puya yakespala Castallanos, RSJ 157 (WIS) Santa Victoria,
Argentina.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 201–224
Kenneth Sytsma