Páramo is the world's fastest evolving and coolest biodiversity hotspot

Abstract

Understanding the processes that cause speciation is a key aim of evolutionary biology. Lineages or biomes that exhibit recent and rapid diversification are ideal model systems for determining these processes. Species rich biomes reported to be of relatively recent origin, i.e., since the beginning of the Miocene, include Mediterranean ecosystems such as the California Floristic Province, oceanic islands such as the Hawaiian archipelago and the Neotropical high elevation ecosystem of the Páramos. Páramos constitute grasslands above the forest tree-line (at elevations of c. 2800-4700 m) with high species endemism. Organisms that occupy this ecosystem are a likely product of unique adaptations to an extreme environment that evolved during the last three to five million years when the Andes reached an altitude that was capable of sustaining this type of vegetation. We compared net diversification rates of lineages in fast evolving biomes using 73 dated molecular phylogenies. Based on our sample, we demonstrate that average net diversification rates of Páramo plant lineages are faster than those of other reportedly fast evolving hotspots and that the faster evolving lineages are more likely to be found in Páramos than the other hotspots. Páramos therefore represent the ideal model system for studying diversification processes. Most of the speciation events that we observed in the Páramos (144 out of 177) occurred during the Pleistocene possibly due to the effects of species range contraction and expansion that may have resulted from the well-documented climatic changes during that period. Understanding these effects will assist with efforts to determine how future climatic changes will impact plant populations.

Full text

ORIGINAL RESEARCH ARTICLE
published: 09 October 2013
doi: 10.3389/fgene.2013.00192
Páramo is the world’s fastest evolving and coolest
biodiversity hotspot
Santiago Madriñán1*, Andrés J. Cortés 1,2 and James E. Richardson1,3
1Laboratorio de Botánica y Sistemática, Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, DC, Colombia
2Evolutionary Biology Centre, Department of Plant Ecology and Genetics, Uppsala University, Uppsala, Sweden
3Tropical Diversity Section, Royal Botanic Garden Edinburgh, Edinburgh, UK
Edited by:
Federico Luebert, Freie Universität
Berlin, Germany
Reviewed by:
Christopher W. Dick, University of
Michigan, USA
Petr Sklenar, Charles University,
Czech Republic
*Correspondence:
Santiago Madriñán, Laboratorio de
Botánica y Sistemática, Universidad
de los Andes, Apartado Aéreo 4976,
Bogotá, DC 111711, Colombia
e-mail: samadrin@uniandes.edu.co
Understanding the processes that cause speciation is a key aim of evolutionary biology.
Lineages or biomes that exhibit recent and rapid diversification are ideal model systems
for determining these processes. Species rich biomes reported to be of relatively recent
origin, i.e., since the beginning of the Miocene, include Mediterranean ecosystems such
as the California Floristic Province, oceanic islands such as the Hawaiian archipelago and
the Neotropical high elevation ecosystem of the Páramos. Páramos constitute grasslands
above the forest tree-line (at elevations of c. 2800–4700 m) with high species endemism.
Organisms that occupy this ecosystem are a likely product of unique adaptations to
an extreme environment that evolved during the last three to five million years when
the Andes reached an altitude that was capable of sustaining this type of vegetation.
We compared net diversification rates of lineages in fast evolving biomes using 73
dated molecular phylogenies. Based on our sample, we demonstrate that average net
diversification rates of Páramo plant lineages are faster than those of other reportedly
fast evolving hotspots and that the faster evolving lineages are more likely to be found in
Páramos than the other hotspots. Páramos therefore represent the ideal model system
for studying diversification processes. Most of the speciation events that we observed
in the Páramos (144 out of 177) occurred during the Pleistocene possibly due to the
effects of species range contraction and expansion that may have resulted from the
well-documented climatic changes during that period. Understanding these effects will
assist with efforts to determine how future climatic changes will impact plant populations.
Keywords: biodiversity hotspots, biogeography, evolutionary radiation, dated molecular phylogenies, net
diversification rates, plant evolution, Páramos
“No zone of alpine vegetation in the temperate or cold parts
of the globe can well be compared with that of the Páramos in
the tropical Andes.” “Nowhere, perhaps, can be found collected
together, in so small a space, productions so beautiful, and so
remarkable in regard to the geography of plants.”
Alexander von Humboldt
Aspects of Nature &Personal narrative
INTRODUCTION
The processes by which lineages diverge into new species are still
poorly understood but are more likely to be determined in lin-
eages that have recently speciated or are undergoing incipient
speciation (Rieseberg and Willis, 2007). Biomes that have numer-
ousexamplesoflineagesthathavespeciatedrecentlyandrapidly
would therefore be ideal places to study evolutionary phenom-
ena. Studies that utilize dated phylogenies have reported high net
diversification rates in a variety of biomes many of which are also
designated biodiversity hotspots (Myers et al., 2000), for example
Succulent Karoo (Klak et al., 2004) or the Mediterranean Basin
(Valente et al., 2010). These radiations may have been caused
by a variety of factors including recent geological activity (e.g.,
Hawaii that is part of the Polynesia-Micronesia hotspot) (Baldwin
and Sanderson, 1998; Price and Wagner, 2004), or recent climatic
change (e.g., Succulent Karoo).
In the Neotropics, lowland forests such as the Amazon have
received a substantial amount of attention as species rich ecosys-
tems (Hoorn et al., 2010). However, the high elevation tropical
Andean Páramo ecosystem is not as widely recognized as a center
of plant diversity. With 3431 species of vascular plants (Luteyn,
1999), Páramos may be considered a hotspot within a hotspot,
as it is located within that of the Tropical Andes (Myers et al.,
2000). Páramos are found at a number of isolated mountain-
tops at altitudes of between 2800 and 4700 m above sea level
forming an archipelago-like distribution between latitudes of
11◦Nand8
◦S covering approximately 35,000 km2(Figure 1).
The physical characteristics of the area occupied by this ecosys-
tem include aseasonal conditions with high daytime and low
nighttime temperatures, continuously high solar energy input,
and high ultraviolet radiation (Luteyn, 1999). The great major-
ity of the plant species found in the Páramos are endemic to
this ecosystem, with close relatives in lowland-tropical or north-
and south-temperate regions (van der Hammen and Cleef, 1986)
(Figure 2). These ecosystems may be considered the “water tow-
ers” of South America as they provide large reservoirs that serve
www.frontiersin.org October 2013 | Volume 4 | Article 192 |1

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
FIGURE 1 | Map indicating the present day area covered by Páramos
(light red).
many of the major Andean cities. Páramos are under threat from
mining activities (gold, coal, and lime) and climate change.
Evolution of the Páramo ecosystem was entirely dependent
on the Andean orogeny as the ecosystem could only have devel-
oped once the Andes had reached a sufficient height. It has been
estimated that the northern Andes reached 40% of its modern ele-
vation from the mid-Miocene/early Pliocene and that they rose
to current heights through rapid final uplift only by around 2.7
million years (Ma) ago (Gregory-Wodzicki, 2000; Mora et al.,
2010). The northern Andes reached the altitude of the mod-
ern tree line that marks the lower limit of Páramo vegetation
near the end of the Pliocene at 2.588 Ma ago (van der Hammen
and Hooghiemstra, 2000). These are therefore the approximate
dates by which conditions suitable for development of the Páramo
ecosystem had established. By the late Pliocene/Early Pleistocene
a proto-páramo vegetation occupied large areas between 2000
and 3000 m (van der Hammen, 1974; Hooghiemstra and van der
Hammen, 2004). This vegetation type was characterized by pollen
of modern Páramo elements such as Poaceae, Vale riana ,Plantago,
Aragoa, Ranunculaceae, Caryophyllaceae, Geranium,Gunnera,
Gentianella and Lysipomia. However, pollen is not sufficiently
diagnostic at species level to determine when speciation in these
groups occurred.
Pleistocene changes in the distribution of this vegetation type
and thus the species that occupy it are evident in the fos-
sil record (van der Hammen, 1974). Individual plant species
may have been forced to migrate vertically and the composi-
tion and distributions of plant communities would thus have
been highly dynamic, with vegetation belts alternately contract-
ing and expanding. During glacial maxima the area of Páramos
was considerably larger than in inter-glacial periods as Páramo
islands occupied lower elevations and thus merged when tem-
peratures were lower (Hooghiemstra et al., 2006). These changes
in distribution, which are largely mediated by temperature fluc-
tuation, are more likely to be greater in a dissected montane
landscape where there are rapid changes in elevation across small
distances. These abiotic conditions would seem to be an ideal
scenario for rapid allopatric speciation and perhaps also permit
more rapid occupation of newly available and novel niche space.
Indeed the Páramos have been characterized by several exam-
ples of rapid diversification events, demonstrated using dated
molecular phylogenies (Särkinen et al., 2012), in genera such
as Gentianella (von Hagen and Kadereit, 2001), Va ler iana (Bell
and Donoghue, 2005), Lupinus (Hughes and Eastwood, 2006)
and Hypericum (Nürk et al., 2013). An increasing amount of
sequence data and calibration points are becoming available per-
mitting the production of dated phylogenies of plant groups from
multiple lineages, allowing a comparison of net diversification
rates amongst hotspots. Here we demonstrate that Páramos are
undergoing an explosive phase of diversification that is both more
rapid and more recent than in any other hotspot.
MATERIALS AND METHODS
DATA AND SAMPLING FOR PÁRAMO LINEAGES
Sequence data generated in the laboratory of the first author or
downloaded from GenBank were assembled and aligned for eight
Páramo genera. Five additional phylogenies, taken from the liter-
ature, of genera containing Páramo clades were also included in
this study (see Supporting Information). Dated phylogenies were
estimated using the software package BEAST 1.4.8 (Drummond
and Rambaut, 2007) using primary or secondary fossil calibra-
tions or in one instance a geological calibration (see below and
Table S1). In instances where these approaches to calibration were
not possible we chose not to apply rates from other studies of
taxa with a similar generation time (generation time has been
showntohaveaneffectonrates)(Richardson et al., 2001; Smith
and Donoghue, 2008) because of the expected elevated muta-
tion rate, resulting from high U.V. light, in high altitude tropical
ecosystems. Age estimates of crown nodes with confidence inter-
vals were then utilized to estimate net diversification rates. Species
and GenBank numbers for sequences used in the study are given
in Appendix S1.
AGES OF CLADES FROM OTHER HOTSPOTS
We compiled data from published dated phylogenetic studies
from Páramo and other hotspots. These used a number of
approaches to date phylogenies and we preferred those results that
used internal fossil primary or secondary calibrations although in
their absence those that used geological calibrations (i.e., oceanic
island emergence) were considered acceptable. We also reported
results of studies in hotspots other than Páramo that used bor-
rowed rates from lineages with similar generation times but did
not include these in our calculations for Páramo studies because,
as mentioned above, we consider species that occupy that ecosys-
tem to have an elevated substitution rate as a result of the
intense U.V. light that is found in tropical highlands. This ele-
vated rate might skew the result in favor of older age estimates
of Páramo lineages. Lineages such as Halenia (Gentianaceae)
Frontiers in Genetics | Evolutionary and Population Genetics October 2013 | Volume 4 | Article 192 |2

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
FIGURE 2 | Plants of the Páramos. Center: Páramo landscape with
Chusquea tessellata (foreground) and Espeletia uribei (background): Frame
(clockwise from top left): Sisyrinchium convolutum,Pterichis habenarioides,
Bomarea pauciflora,Puya trianae,Oreobolus goeppingeri,Paepalanthus
alpinus,Berberis goudotii,Ranunculus peruvianus,Echeveria bicolor,
Hypericum goyanesii,Lachemilla orbiculata,Gaultheria anastomosans,
Gentiana sedifolia,Halenia major,Lupinus alopecuroides,Aragoa abietina,
Bartsia laniflora,Eryngium humboldtii,Myrrhidendron glaucescens,
Diplostephium phylicoides,Hypochoeris sessiliflora,Espeletia killipii,
Lysipomia laciniata and Valeriana stenophylla.
should therefore actually have a higher net diversification rate
than we would estimate by applying the fastest reported rate for
herbaceous annuals.
If alternative options were available the date chosen was
the one that was calibrated using fossils rather than geological
events due to problems with the latter approach highlighted by
Renner (2005). As different dates result from different analyti-
cal approaches we favored dates calculated by Bayesian methods
followed by penalized likelihood and then NPRS (the latter has
been shown to over-estimate ages) (Lavin et al., 2005). Favoring
of Bayesian age estimates also permitted a more direct compari-
son with results of our analyses of Páramo lineages all of which
used that approach.
Species numbers of Heliophila in each hotspot were taken
from Marais (1970). The age reported for Kokia is that of the
stem node and therefore an underestimate of the rate presented.
Mediterranean studies of Geranium and Erodium are possible
underestimates as only endemic species were included but those
studies also included species outsidethe Mediterranean basin that
we were unable to exclude because of a lack of distribution infor-
mation. In some cases it was difficult to assess actual numbers
of species of lineages in other biomes, e.g., Fabaceae lineages in
the Cape Floristic Region likely have species that occur outside of
that region. In some of our examples we included all species in a
genusinourestimatesevenwhenitislikelythatnotallspecies
are found within that biome which means we are overestimating
net diversification rates in those lineages.
DETERMINATION OF AGES OF PÁRAMO CLADES
A Bayesian dating method with a relaxed molecular clock was
implemented using the program BEAST 1.4.8 (Drummond and
Rambaut, 2007) to estimate divergence times. An XML (eXtensi-
ble Mark-up Language) input file was generated in the Bayesian
Evolutionary Analysis Utility software (BEAUti) version v.1.4.8
(Drummond and Rambaut, 2007) (XML files for each analysis
are available upon request to the corresponding author). The
www.frontiersin.org October 2013 | Volume 4 | Article 192 |3

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
FIGURE 3 | Comparison of net diversification rates (r) in fast evolving
biodiversity hotspots. Upper (triangle), lower (diamond), mean (square)
and Standard Deviation around the mean net diversification rates (Y axis)
for each hotspot. Sample sizes: Páramos n=13; Mediterranean Floristic
Province n=8; Succulent Karoo n=9; Hawaiian Archipelago n=9;
Cerrado n=10; Cape Floristic Region n=13; California Floristic Province
n=6; Southwest Australia n=5; All Regions n=73.
best performing evolutionary model was identified under two
different model selection criteria, the hierarchical likelihood ratio
test (hLRT) and the Akaike information criterion as implemented
in MrModelTest (Nylander, 2004). Both selection criteria indi-
catedthatforeachdatasetaGeneralTimeReversible(GTR)
with site heterogeneity being gamma distributed and with invari-
ant sites model was optimal. An uncorrelated lognormal relaxed
clock model was chosen based on the assumption of the absence
of a molecular clock. To specify informative priors for all the
parameters in the model, the Yule tree prior was used that was
recommended as being appropriate for species-level phylogenies
(Ho, 2007). As also recommended by Ho (2007),alognormal
prior distribution was applied to fossil based calibrations and
a normal distribution was used for secondary calibrations. The
XML file was run in BEAST 1.4.8 (Drummond and Rambaut,
2007). Two runs were performed for each analysis. The MCMC
chain length was set to 10,000,000, to screen every 10,000 and
sample every 1000 trees. The resulting log file was imported
into Tracer to check whether ESS values were adequate for each
parameter. If they were not additional runs of 10,000,000 genera-
tions were performed until adequate ESS values were achieved.
LogCombiner (Drummond and Rambaut, 2007)wasusedto
combine tree files in cases where multiple runs were necessary.
TreeAnnotator (Drummond and Rambaut, 2007)wasusedto
produce the maximum clade credibility (MCC) tree that has the
maximum sum of posterior probabilities on its internal nodes
and summarizes the node height statistics in the posterior sample.
MCC files were visualized using FigTree version 1.2.3 (Rambaut,
2009) and median and 95% highest posterior density (HPD) ages
are reported in Table S1. We also calculated the number of species
that, based on their median ages, diverged from their MRCA dur-
ing the Pleistocene, i.e., within the last 2.58 million years, for each
Páramo lineage.
CALCULATION OF NET DIVERSIFICATION RATES
There are a number of diversification rate measures but we report
that of the simple estimator of Kendall (1949) and Moran (1951)
where r=ln(N)−ln(N0)]/T(where N=standing diversity, N0
=initial diversity, here taken as =1, and T=inferred clade age).
This estimate, a pure-birth model of diversification with a con-
stant rate and no extinction, is the same as that of Magallón and
Sanderson (2001).
STATISTICAL ANALYSES
Average net diversification rates of all lineages within hotspots
were calculated and a 95% bootstrap interval, using 1000 iter-
ations, around each mean diversification rate was determined
for each hotspot. Number of species, crown node age, mean
diversification rate and number of Pleistocene speciation events
for each Páramo lineage in the study are indicated in Ta b l e 1
(chronograms for each study are indicated in Figures S1A–H;
Table S1 includes data on taxa from other hotspots).
Re-sampling without replacement was carried out 1000 times
in order to estimate the probability that the fastest evolving lin-
eage comes from a particular region. In each re-sampling step,
five lineages per hotspot were randomly chosen across the eight
hotspots, and the region where the fastest evolving lineage came
from was identified from the 40 total randomly chosen lineages.
The numbers of consecutive fastest evolving lineages that belong
to the same region were also recorded. Two summary statistics per
hotspot were calculated based on the 1000 sampling processes:
the proportion of cases where the fastest evolving lineage came
from a particular region and the maximum number of consecu-
tive fastest evolving lineages that belong to the same region. Mean
and confidence intervals for these two summary statistics were
calculated running 1000 independent iterations of 1000 samples
each. The summary statistics, their means and their confidence
intervals are presented in Table S2.
RESULTS
Páramo lineages have higher net diversification rates than the
fastest known lineages in other hotspots and have the fastest
mean diversification rate of all hotspots (Figure 3;Ta b l e 2 ).
The average diversification rate of the Páramo lineages sampled
(Ta b l e s 1 ,2) is 1.36 speciation events per million years (Myr-1;
n=13; we report values for a pure-birth model of diversifica-
tion, one with a constant rate and no extinction r(Kendall, 1949;
Moran, 1951; Magallón and Sanderson, 2001)(seeCalculation
of net diversification rates in methods above); rates factoring in
extinction are reported in Table S1) compared with 1.07 Myr-
1intheMediterraneanBasin(n=8), 0.76 Myr-1 in Succulent
Karoo (n=9), 0.73 Myr-1 in Hawaii (n=9), 0.58 Myr-1 in
Cerrado (n=10), 0.40 Myr-1 in the Cape Floristic Region (n=
13), 0.39 Myr-1 in the California Floristic Province (n=6)
Frontiers in Genetics | Evolutionary and Population Genetics October 2013 | Volume 4 | Article 192 |4

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
Table 1 | Net diversification rates of Páramo plant lineages.
Crown node age (Ma) Net diversification Rate (r)
Lineage Family nCalibration
node
Calibration
age (Ma)
Minimum Mean Maximum Minimum Mean Maximum No. of
Pleistocene
speciations
Aragoa Plantaginaceae 17 Island
Plantago
0.60 0.12 0.42 0.92 17.83 5.10 2.33 5 of 5
Arcytophyllum Rubiaceae 14 Arcytophyllum
stem node
21.50 6.48 10.96 16.36 0.30 0.18 0.12 1of 11
Berberis Berberidaceae 32 Crown node
of Berberis
37.30 0.07 3.80 9.7 39.61 0.73 0.29 4 of 17
Calceolaria Calceolariaceae 65 Jovellana/
Calceolaria
split
15.00 1.42 2.50 3.51 2.45 1.39 0.99 23 of 23
Draba Brassicaceae 55 Brassicaceae
crown node
37.60 1.60 3.05 4.12.07 1.09 0.81 23 of 24
Espeletiinae Asteraceae 120 Barnadesia
split
45.70 2.42 4.04 5.92 1.69 1.01 0.69 21 of 22
Festuca Poaceae 36 Loliinae crown
node
13.80 1.87 4.28 7.66 1.55 0.68 0.38 3 of 5
Jamesonia +
Eriosorus
Pteridaceae 32 Multiple
fossils
7.60 n.a. 7.60 n.a. n.a. 0.36 n.a. 0 of 2
Lupinus Fabaceae 66 Lupinus/
Spartium split
16.01 1 .18 1.47 1.76 2.96 2.38 1.99 32 of 32
Lysipomia Campanulaceae 27 Lysipomia
crown node
11.10 6.61 8.96 11.19 0.39 0.29 0.23 13 of 20
Oreobolus Cyperaceae 5 O. furcatus 5.10 1.67 3.01 4 .71 0.55 0.30 0.19 3 of 5
Puya Bromeliaceae 46 Puya stem
node
9.10 0.26 0.80 1.58 12.06 3.92 1.98 10 of 10
Valeria na Valerianaceae 53 Valerianaceae
crown
55.00 9.46 14.58 19.69 0.35 0.22 0.17 n.a.
n, number of species within lineage; n.a., not available; Ma, million years ago.
and 0.14 Myr-1 in Southwest Australia (n=5). There are iso-
lated lineages in some hotspots that have high rates such as
in Dianthus (Valente et al., 2010)andcoreRuschioideae(Klak
et al., 2004). However, the average rate is significantly higher
in Páramos than it is for a random sample of 13 from within
our dataset of all hotspots. We also show that the fastest evolv-
ing lineage has a greater probability of being from the Páramos
(0.51) than from any other hotspot (0.40 for the Mediterranean
and 0.02 for Succulent Karoo; Table S2). The average number
of fastest lineages that belong to the same region is also great-
est in Páramos. In addition to the rapid net diversification rates,
Páramos have a very high species density in comparison to other
hotspots with 3431 species, nearly all of which occur nowhere
else. Ta b l e 2 indicates the values for other hotspots and also that
although the Cape Floristic Region has more species per kilome-
ter squared than Páramos, the average rate per area in Páramos
is greater than the Cape Floristic Region and all other hotspots
studied.
DISCUSSION
We demonstrate that Páramos not only have had a rapid diver-
sification rate but those radiations have also been more recent
than in other hotspots. In addition these diversifications have
occurred more or less over the same period of time in multiple
unrelated lineages in contrast to, for example, the single rapid
diversification of cichlid fishes that occurred in a restricted area in
East African lakes (Kornfield and Smith, 2000). Additional recent
studies of evolutionary histories are also consistent with the rapid
diversification of other Páramo lineages (Vargas and Madriñán,
2012; Nürk et al., 2013). Because Páramo lineages are in an early
explosive phase of diversification we expect current species com-
position to be the result of on-going speciation processes with
extinction having a minimal effect. Possible causes of diversifica-
tion in Páramos include allopatric speciation resulting from dis-
tribution changes caused by climatic cycles during the Pleistocene
or, adaptation to numerous new microclimates and substrates
resulting from geological activity associated with Andean uplift.
We acknowledge that diversification of some lineages may have
occurred prior to the Plio-Pleistocene. However, our chrono-
grams indicate that, based on median ages, 144 of the 176 Páramo
species in our study split from their MRCA during the Pleistocene
(Ta b l e 1 ) that is consistent with them having arisen as a result
of inter-glacial range contractions in that epoch. We assume that
the addition of more species to our sample will increase this fig-
ure. Although allopatric speciation could be the primary cause of
isolation, the high levels of ultraviolet light are likely to induce
www.frontiersin.org October 2013 | Volume 4 | Article 192 |5

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
Table 2 | Biodiversity Hotspots species richness and mean net diversification rates.
Region Area No. of No. of Mean Net Speciation events per
(km2) species species/km2Diversification million years per
(endemics) rate km2
California Floristic Province 293,804 8000 (2124) 0.027 0.39 1.32 ×10−6
Cape Floristic Region 78,555 9000 (6210) 0.196 0.40 5.05 ×10 −6
Cerrado 2,031,990 12,669 (4215) 0.060 0.58 0.29 ×10−6
Hawaiian Archipelago 28,311 1004 (c.900) 0.035 0.73 25.68 ×10 −6
Mediterranean Floristic Province 2,085,292 22,500 (11,700) 0.010 1.07 0.52 ×10−6
Páramos 35,000 3431 (*)0.098 1.36 38.80 ×10−6
Southwest Australia 356,717 5500 (2948) 0.015 0.14 0.38 ×10 −6
Succulent Karoo 102,691 6350 (2439) 0.062 0.76 7.38 ×10−6
*Precise number of endemic species unknown, but close to 100%.
a rapid mutation rate (Davies et al., 2004; Willis et al., 2009),
and therefore hasten morphological differentiation and perhaps
reproductive isolation with these mutations being more likely to
become fixed in small fragmented populations. It is also possible
that ecological opportunity and physiographic heterogeneity were
the primary factors driving rapid diversification, e.g., Andean
Lupinus (Hughes and Eastwood, 2006). The actual processes of
speciation remain unclear, however, what is evident from this
study is that it occurred more rapidly in Páramos than in any
other hotspot on earth and confirms Hughes and Eastwood’s
(2006) prediction that the species-richness of the flora is the result
of a set of rapid plant radiations.
Species that occupy steep altitudinal gradients are likely to
undergo altitudinal range shifts with changes in temperature and
are therefore ideal organisms to model the effects of historical
and potential future changes. High altitude restricted species are
also the most threatened due to the limited areas into which they
can migrate under conditions of increasing temperatures such as
those we are currently experiencing. The relatively small areas
of Páramo vegetation make them logistically easier to study. For
example, fragmented areas of Páramos around Bogotá that are as
little as 30 km apart and would likely (based on palaeobotanical
evidence from the Sabana de Bogotá (van der Hammen, 1973,
1974; van der Hammen and Cleef, 1986) have been connected
during the last glacial maximum may be studied to look for sig-
natures of fragmentation processes that occurred within the last
10,000 years and in previous inter-glacial periods.
When faced with changing climatic conditions, such as tem-
perature increases, populations respond either by adapting, going
extinct or migrating (Fordham et al., 2012). The contraction
and expansion of populations that is very evident in Páramos
according to palaeoecological data (van der Hammen, 1974;
Hooghiemstra and van der Hammen, 2004), and that could have
resulted in the high number of Pleistocene speciation events
reported here, is indicative of an inability to adapt to changing
conditions, as demonstrated in other montane systems (Colwell
et al., 2008; Kelly and Goulden, 2008; Lenoir et al., 2008). This
inability to adapt over periods of thousands of years reinforces
the dangers that plant populations face in these environments
when challenged by changes that might occur over shorter time
scales of decades or centuries. Research into Páramo plants will
help us to understand past and future evolutionary processes and
provide the information necessary to help to conserve this and
other ecosystems in the face of the continuing pressures exerted
by anthropogenic climatic alterations.
ACKNOWLEDGMENTS
Thanks to Tony Verboom, Klaus Mummenhoff, Peter Goldblatt,
Freek Bakker, Peter Linder, Jenny Archibald, Chloe Galley and
Felix Forest for supplying accurate dates and/or species num-
bers for Cape/Succulent Karoo and Mike Crisp for supplying
accurate dates and species numbers for Southwest Australian lin-
eages. Juan José Aldasoro is thanked for additional information
on Geraniaceae node ages and thanks to Isabel Sanmartín for help
with other Mediterranean studies. Diego Riaño is thanked for
help with BEAST analyses. Thanks to Michael Donoghue, Colin
Hughes, Kyle Dexter and the Royal Botanic Garden Edinburgh
Journal Club for comments on the manuscript. Bhaskar Adhikari
(RBGE) and Maria Pinilla (Universidad de Los Andes) are
thanked for use of unpublished data. We are gratefull to Fernando
SalazarfortheproductionofthemapofthePáramos.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online
at: http://www.frontiersin.org/journal/10.3389/fgene.2013.00192/
abstract
REFERENCES
Baldwin, B. G., and Sanderson, M. J.
(1998). Age and rate of diversifi-
cation of the Hawaiian silversword
alliance (Compositae). Proc. Natl.
Acad. Sci. U.S.A. 95, 9402–9406. doi:
10.1073/pnas.95.16.9402
Bell, C. D., and Donoghue, M. J. (2005).
Phylogeny and biogeography of
the Valerianaceae (Dipsacales)
with special reference to the
South American valerians. Org.
Divers. Evol. 5, 147–159. doi:
10.1016/j.ode.2004.10.014
Colwell, R. K., Brehm, G., Cardelús, C.,
Gilman,A.C.,andLongino,J.T.
(2008). Global warming, elevational
range shifts, and lowland biotic
attrition in the wet tropics. Science
322, 258–261. doi: 10.1126/science.
1162547
Davies, T. J., Savolainen, V., Chase,
M. W., Moat, J., and Barraclough,
T. G. (2004). Environmental
energy and evolutionary rates
in flowering plants. Proc. R.
Soc.Lond.BBiol.Sci.271,
2195–2200. doi: 10.1098/rspb.
2004.2849
Drummond, A. J., and Rambaut, A.
(2007). BEAST: bayesian evolution-
ary analysis by sampling trees. BMC
Evol. B iol. 7:214. doi: 10.1186/1471-
2148-7-214
Fordham,D.A.,Resit,H.Akaya,A.K.
C., Araújo, M. B., Elith, J., Keith,
Frontiers in Genetics | Evolutionary and Population Genetics October 2013 | Volume 4 | Article 192 |6

Madriñán et al. Páramos, a fast-evolving biodiversity hotspot
D. A., et al. (2012). Plant extinc-
tion risk under climate change: are
forecast range shifts alone a good
indicator of species vulnerability to
global warming? Glob. Chang. Biol.
18, 1357–1371. doi: 10.1111/j.1365-
2486.2011.02614.x
Gregory-Wodzicki, K. M. (2000).
Uplift history of the Central and
Northern Andes: a review. Geol.
Soc. Am. Bull. 112, 1091–1105.
doi: 10.1130/0016-7606(2000)112<
1091:UHOTCA>2.0.CO;2
Ho, S. Y. M. (2007). Calibrating molec-
ular estimates of substitution rates
and divergence times in birds.
J. Avian. Biol. 38, 409–414. doi:
10.1111/j.2007.0908-8857.04168.x
Hooghiemstra, H., and van der
Hammen, T. (2004). Quaternary
Ice-Age dynamics in the Colombian
Andes: developing an understand-
ing of our legacy. Philos. Trans. R.
Soc. Lond. B Biol. Sci. 359, 173–181.
doi: 10.1098/rstb.2003.1420
Hooghiemstra, H., Wijninga, V., and
Cleef, A. (2006). The palaeob-
otanical record of Colombia:
implications for biogeography and
biodiversity. Ann. Mo. Bot. Gard. 93,
297–325. doi: 10.3417/0026-6493
(2006)93 [297:TPROCI]2.0.CO;2
Hoorn, C., Wesselingh, F. P., ter Steege,
H., Bermudez, M. A., Mora, A.,
Sevink, J., et al. (2010). Amazonia
through time: andean u plift, climate
change, landscape evolution, and
biodiversity. Science 330, 927–931.
doi: 10.1126/science.1194585
Hughes, C., and Eastwood, R. (2006).
Island radiation on a continen-
tal scale: exceptional rates of plant
diversification after uplift of the
Andes. Proc. Natl. Acad. Sci. U.S.A.
103, 10334–10339. doi: 10.1073/
pnas.0601928103
Kelly, A., and Goulden, M. (2008).
Rapid shifts in plant distribu-
tion with recent climate change.
Proc. Natl. Acad. Sci. U.S.A. 105,
11823–11826. doi: 10.1073/pnas.
0802891105
Kendall, D. G. (1949). Stochastic pro-
cesses and population growth. J. R.
Stat. Soc. B Stat. Methodol. 11,
230–264.
Klak, C., Reeves, G., and Hedderson, T.
(2004). Unmatched tempo of evolu-
tion in southern African semi -desert
ice plants. Nature 427, 63–65. doi:
10.1038/nature02243
Kornfield, I., and Smith, P. F. (2000).
African Cichlid fishes: model
systems for evolutionary biology.
Annu. Rev. Ecol. Evol. Syst. 31,
163–196. doi: 10.1146/annurev.
ecolsys.31.1.163
Lavin, M., Herendeen, P., and
Wojciechowski, M. F. (2005).
Evolutionary rates analysis of
Leguminosae implicates a rapid
diversification of lineages during
the Tertiary. Syst. Biol. 54, 530–549.
doi: 10.1080/10635150590947131
Lenoir, J., Gégout, J. C., Marquet, P.
A.,deRuffray,P.,andBrisse,H.
(2008). A significant upward shift
in plant species optimum eleva-
tion during the 20th century. Science
320, 1768–1771. doi: 10.1126/sci-
ence.1156831
Luteyn, J. L. (1999). Páramos: a
Checklist of Plant Diversity,
Geographic Distribution and
Botanical Literature.NewYork,NY:
The New York Botanical Garden
Press.
Magallón, S., and Sanderson, M.
J. (2001). Absolute diversifica-
tion rates in angiosperm clades.
Evolution 55, 1762–1780. doi:
10.1554/0014-3820(2001)055[1762:
ADRIAC]2.0.CO;2
Marais, W. (1970). “Heliophila,” in
Flora of Southern Africa, Vol. 13, eds
L. E. Codd, B. de Winter, D. J. B.
Killick, and H. B. Rycroft (Pretoria:
Botanical Research Institute),
17–77.
Mora, A., Baby, P., Roddaz, M., Parra,
M.,Brusset,S.,Hermoza,W.,
et al. (2010). “Tectonic history
of the Andes and sub-Andean
zones: implications for the devel-
opment of the Amazon drainage
basin,” in Amazonia: Landscape and
Species Evolution, eds C. Hoorn
and F. Wesselingh (Chichester:
Wiley-Blackwell), 38–60.
Moran, P. A. (1951). Estimation meth-
ods for evolutive processes. J. R.
Stat. Soc. B Stat. Methodol. 13,
141–146.
Myers, N., Mittermeier, R. A.,
Mittermeier, C. G., da Fonseca,
G. A. B., and Kent, J. (2000).
Biodiversity hotspots for conserva-
tion priorities. Nature 403, 853–858.
doi: 10.1038/35002501
Nürk, N. M., Scheriau, C., and
Madriñán, S. (2013). Explosive
radiation in high Andean
Hypericum—rates of diversifi-
cation among New World lineages.
Front. Genet. 4:175. doi: 10.3389/
fgene.2013.00175
Nylander, J. A. A. (2004). MrModeltest
v2. Available online at: https://
github.com/nylander/MrModeltest2
Price, J. P., and Wagner, W. L. (2004).
Speciation in Hawaiian angiosperm
lineages: cause, consequence and
mode. Evolution 58, 2185–2200. doi:
10.1554/03-498
Rambaut, A. (2009). FigTree v1.2.3.
Available online at: http://tree.bio.
ed.ac.uk/software/figtree
Renner, S. S. (2005). Relaxed molecu-
lar clocks for dating historical plant
dispersal events. Trends Plant Sci.
10, 550–558. doi: 10.1016/j.tplants.
2005.09.010
Richardson, J. E., Pennington,
R. T., Pennington, T. D., and
Hollingsworth, P. M. (2001). Rapid
diversification of a species-rich
genus of neotropical rain forest
trees. Science 293, 2242–2245. doi:
10.1126/science.1061421
Rieseberg, L. H., and Willis, J. H.
(2007). Plant speciation. Science
317, 910–914. doi: 10.1126/science.
1137729
Särkinen, T., Pennington, R. T., Lavin,
M.,Simon,M.F.,andHughes,C.
E. (2012). Evolutionary islands in
the Andes: persistence and isolation
explain high endemism in Andean
dry tropical forests. J. Biogeogr. 39,
884–900. doi: 10.1111/j.1365-2699.
2011.02644.x
Smith, S. A., and Donoghue, M. J.
(2008). Rates of molecular evolu-
tion are linked to life history in flow-
ering plants. Science 322, 86–89. doi:
10.1126/science.1163197
Valente, L. M., Savolainen, V., and
Vargas, P. (2010). Unparalleled rates
of species diversification in Europe.
Proc. R. Soc. Lond. B Biol. Sci. 277,
1489–1496. doi: 10.1098/rspb.2009.
2163
van der Hammen, T. (1973). The
Quaternary of Colombia: intro-
duction to a research project and a
series of publications. Pa lae ogeo gr.
Palaeoclimatol. Palaeoecol. 14,
1–7. doi: 10.1016/0031-0182(73)
90063-1
van der Hammen, T. (1974). The
Pleistocene changes of vegetation
and climate in tropical South
America. J. Biogeogr. 1, 3–26. doi:
10.2307/3038066
van der Hammen, T., and Cleef, A.
M. (1986). “Development of the
high Andean Páramo flora and veg-
etation,” in High Altitude Tropical
Biogeography, eds F.Vuilleumier and
M. Monasterio (Oxford: Oxford
University Press), 153–201.
van der Hammen, T., and
Hooghiemstra, H. (2000). Neogene
and Quaternary history of vege-
tation, climate and plant diversity
in Amazonia. Quat. Sci. Rev. 19,
725–742. doi: 10.1016/S0277-3791
(99)00024-4
Vargas, O. M., and Madriñán, S.
(2012). Preliminary phylogeny of
Diplostephium (Asteraceae): specia-
tion rate and character evolution.
Lundlellia 15, 1–15.
von Hagen, K. B., and Kadereit, J.
W. (2001). The phylogeny of
Gentianella (Gentianaceae) and its
rapid colonization of the southern
hemisphere as revealed by nuclear
and chloroplast DNA sequence
variation. Org. Divers. Evol. 1,
61–79. doi: 10.1078/1439-6092-
00005
Willis, K. J., Bennett, K. D., and Birks,
H. J. B. (2009). Variability in
thermal and UV-B energy fluxes
through time and their influence
on plant diversity and speciation.
J. Biogeogr. 36, 1630–1644. doi:
10.1111/j.1365-2699.2009.02102.x
Conflict of Interest Statement: The
authors declare that the research
was conducted in the absence of any
commercial or financial relationships
that could be construed as a potential
conflict of interest.
Received: 28 May 2013; accepted: 08
September 2013; published online: 09
October 2013.
Citation: Madriñán S, Cortés AJ and
Richardson JE (2013) Páramo is the
world’s fastest evolving and coolest biodi-
versity hotspot. Front. Genet. 4:192. doi:
10.3389/fgene.2013.00192
This article was submitted to
Evolutionary and Population Genetics,
a section of the journal Frontiers in
Genetics.
Copyright © 2013 Madriñán, Cortés
and Richardson. This is an open-access
article distributed under the terms of the
Creative Commons Attribution License
(CC BY). The use, distribution or repro-
duction in other forums is permitted,
provided the original author(s) or licen-
sor are credited and that the original
publication in this journal is cited, in
accordance with accepted academic prac-
tice. No use, distribution or reproduction
is permitted which does not comply w ith
these terms.
www.frontiersin.org October 2013 | Volume 4 | Article 192 |7