ORIGINAL RESEARCH ARTICLE
published: 09 October 2013
Páramo is the world’s fastest evolving and coolest
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
Federico Luebert, Freie Universität
Christopher W. Dick, University of
Petr Sklenar, Charles University,
Santiago Madriñán, Laboratorio de
Botánica y Sistemática, Universidad
de los Andes, Apartado Aéreo 4976,
Bogotá, DC 111711, Colombia
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
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-
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
◦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
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
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)
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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
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
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
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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-
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
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
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.
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)
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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
Minimum Mean Maximum Minimum Mean Maximum No. of
Aragoa Plantaginaceae 17 Island
0.60 0.12 0.42 0.92 17.83 5.10 2.33 5 of 5
Arcytophyllum Rubiaceae 14 Arcytophyllum
21.50 6.48 10.96 16.36 0.30 0.18 0.12 1of 11
Berberis Berberidaceae 32 Crown node
37.30 0.07 3.80 9.7 39.61 0.73 0.29 4 of 17
Calceolaria Calceolariaceae 65 Jovellana/
15.00 1.42 2.50 3.51 2.45 1.39 0.99 23 of 23
Draba Brassicaceae 55 Brassicaceae
37.60 1.60 3.05 4.12.07 1.09 0.81 23 of 24
Espeletiinae Asteraceae 120 Barnadesia
45.70 2.42 4.04 5.92 1.69 1.01 0.69 21 of 22
Festuca Poaceae 36 Loliinae crown
13.80 1.87 4.28 7.66 1.55 0.68 0.38 3 of 5
Pteridaceae 32 Multiple
7.60 n.a. 7.60 n.a. n.a. 0.36 n.a. 0 of 2
Lupinus Fabaceae 66 Lupinus/
16.01 1 .18 1.47 1.76 2.96 2.38 1.99 32 of 32
Lysipomia Campanulaceae 27 Lysipomia
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
9.10 0.26 0.80 1.58 12.06 3.92 1.98 10 of 10
Valeria na Valerianaceae 53 Valerianaceae
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
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
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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.
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
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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
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:
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