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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.
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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
11Nand8
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
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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)
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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
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
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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-
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)
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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
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
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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 ×106
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 ×106
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 ×106
Páramos 35,000 3431 (*)0.098 1.36 38.80 ×106
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 ×106
*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
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abstract
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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
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
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www.frontiersin.org October 2013 | Volume 4 | Article 192 |7
... The Neotropical páramo, a high-altitude ecosystem at an elevation of about 2,800-4,700 m, is a species-rich biome of the relatively recent Miocene origin and is characterized by high species endemism and fast speciation rate (Madriñán et al. 2013). By comparing diversification rates of lineages in fast evolving biomes and by using numerous molecular phylogenies, it has been found that average diversification rates of páramo lineages are faster than those of other reportedly fast evolving biodiversity hotspots (Madriñán et al. 2013). ...
... The Neotropical páramo, a high-altitude ecosystem at an elevation of about 2,800-4,700 m, is a species-rich biome of the relatively recent Miocene origin and is characterized by high species endemism and fast speciation rate (Madriñán et al. 2013). By comparing diversification rates of lineages in fast evolving biomes and by using numerous molecular phylogenies, it has been found that average diversification rates of páramo lineages are faster than those of other reportedly fast evolving biodiversity hotspots (Madriñán et al. 2013). In the páramo, organisms that populate this ecosystem are a likely product of specific adaptations to an extreme environment that evolved during the Pleistocene or the last three to five million years (Madriñán et al. 2013, Stonis et al. 2016. ...
... By comparing diversification rates of lineages in fast evolving biomes and by using numerous molecular phylogenies, it has been found that average diversification rates of páramo lineages are faster than those of other reportedly fast evolving biodiversity hotspots (Madriñán et al. 2013). In the páramo, organisms that populate this ecosystem are a likely product of specific adaptations to an extreme environment that evolved during the Pleistocene or the last three to five million years (Madriñán et al. 2013, Stonis et al. 2016. Thus, according to Madriñán et al. (2013), the páramo represents an ideal model ecosystem for investigating diversification processes. ...
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... It has been suggested that changes in the composition of plant communities along altitudinal gradients may be determined by environmental filtering, since increasing altitudes are often associated with harsh conditions for life (Laiolo & Obeso, 2017). Hence, only a relatively low number of species have been capable of adapting to the prevailing abiotic conditions at high altitudes, resulting in a general decline in species richness but an increase in endemism (Billings, 1974;Rada, Azócar & García-Núñez, 2019;Madriñán, Cortés & Richardson, 2013). In the Neotropics, the Paramo exemplifies a high elevation ecosystem; this habitat is typically composed of low herbaceous and shrubby vegetation whose physiognomy drastically contrasts with the arboreal vegetation that dominates the adjacent Montane Forests (Smith & Young, 1987;Luteyn, 2005). ...
... Most of the neotropical Paramos (including the Puna) are found in South America and cover a large proportion of the highlands of the Andes mountain range (Madriñán, Cortés & Richardson, 2013). In Central America, the Paramo vegetation is restricted to highly isolated and small natural fragments on the highlands of the Talamanca mountain range that extends from Costa Rica to western Panama (Kappelle & Horn, 2016). ...
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... These regions are characterized by peculiar and harsh environmental and ecological conditions: high daily temperature fluctuations (with sub-zero temperatures during the night and relatively high temperatures during the day), high radiation (solar and UV), and fast changes in radiation and physiological dryness (Luteyn, 1999). They are listed, as part of the Andes Biodiversity Hotspot, among the global biodiversity hotspots (Myers et al., 2000;Madriñán et al., 2013;Testolin et al., 2020). The páramo hotspot is exceptional in that it is characterized by the world's fastest plant diversification rates, high endemism and high regional species richness (Madriñán et al., 2013;Testolin et al., 2021). ...
... They are listed, as part of the Andes Biodiversity Hotspot, among the global biodiversity hotspots (Myers et al., 2000;Madriñán et al., 2013;Testolin et al., 2020). The páramo hotspot is exceptional in that it is characterized by the world's fastest plant diversification rates, high endemism and high regional species richness (Madriñán et al., 2013;Testolin et al., 2021). In addition, páramos provide several ecosystem services such as carbon storage and water supply for cities, agriculture and hydropower (Buytaert et al., 2011). ...
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... Montane vegetation formations worldwide often have exceptional species richness and endemism, and so are the subjects of numerous studies on diversification dynamics (reviewed by Rahbek et al., 2019). Most studies focus on aspects of montane landscapes that can accelerate speciation and increase local endemism, such as the altitudinal gradient and that mountaintops create continental archipelago-like systems (also known as "sky-islands") that impose frequent barriers to gene flow (Madriñán et al., 2013;Merckx et al., 2015;Antonelli, 2015;Hoorn et al., 2018). Exceptional rates of speciation have also been linked to the process of orogeny itself (Hughes and Eastwood, 2006, but see Vasconcelos et al., 2020). ...
... The age and speed of diversification of montane lineages is often linked to the geological history of the mountain range itself, with faster diversification expected to be found in younger montane systems (e.g. Madriñán et al., 2013;Merckx et al., 2015). However, there is a gap in studies comparing the diversification dynamics of closely related lineages that are endemic to montane systems of different geological ages. ...
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... Previous studies indicate that diversification rates might be structured geographically in the Neotropics (Harvey et al., 2020;Jetz et al., 2012;Quintero and Jetz, 2018;Rangel et al., 2018), with geography and climate being strong predictors of evolutionary rate variation (Quintero and Jetz, 2018;Rangel et al., 2018). For example, speciation may be high in regions subject to environmental perturbations, such as orogenic activity (Esquerré et al., 2019;Lagomarsino et al., 2016;Vasconcelos et al., 2020;Pouchon et al., 2018;Madriñán et al., 2013), and often not associated with current species richness (Harvey et al., 2020;Quintero and Jetz, 2018). Still, little is known on the geographic structure of long-term Neotropical diversification. ...
... This opposite pattern suggests that Cenozoic environmental changes drove diversification slowdowns for some tetrapods, but stimulated plant diversification. Although Neotropical climate has been relatively stable through the Cenozoic in comparison to other regions (Ziegler et al., 2003;Morley, 2007), in the Neotropics, global cooling contributed to the expansion of several biomes, such as the alpine Paramos (Madriñán et al., 2013) and other open ecosystems (Cheng et al., 2013;Dick and Pennington, 2019), providing new opportunities for diversification. Higher mean speciation rates in plants than in tetrapods (Figure 8) could have provided plant lineages more opportunities for adaptation to changing environments (Hughes and Eastwood, 2006). ...
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... Kilimanjaro (Hughes & Eastwood, 2006;Madriñán et al., 2013;Molina-Venegas et al., 2020) and mountains on islands such as Mt. Kinabalu (Merckx et al., 2015). ...
Thesis
Global change is putting unprecedented pressure on plants to adapt or migrate to avoid extinction. Studying the past responses of plants to environmental change can shed light on the potential evolutionary outcomes and sensitivity of species to future environmental change. These processes are especially relevant to highly diverse, evolutionarily rich, and ecologically vulnerable alpine ecosystems. My PhD aims to narrow the uncertainty about how plant lineages with a range of lowland and alpine species will be impacted by global change by studying the historical biogeography, trait and species diversification, and ecological strategies of alpine species in a phylogenetic framework. Chapter 1 reviews current knowledge about the relative roles of migration and adaptation in plant responses to climate change and how historical biogeographical and evolutionary modeling provide novel insights to these questions. Chapter 2 applies recent developments in sequencing methods to construct a new, near-complete phylogeny of a diverse species radiation, New Zealand Veronica, also addressing questions about how to resolve difficulties in reconstructing phylogenetic relationships in recent, rapid radiations such as Veronica. This group serves as an important case study for further evolutionary questions about the relationships between habitat, species diversity, and environmental change. Chapter 3 estimates the contributions of in situ cladogenesis (i.e., the formation of new species) and colonization from lowland habitat in generating mountain diversity in Veronica. Further, the chapter explores the importance of niche adaptation and divergence in contributing to cladogenesis, and presents a general, conceptual model to understand how mountain diversity accumulates. Chapter 4 compares the potential range and niche change required for plant species to respond to future climate change relative to the change undergone since the mid-Holocene. It also determines which niche traits can predict “winners” and “losers” under climate change. Chapter 5 discusses the main findings of the thesis and ends with proposed avenues for future research.
... Global warming is predicted to severely affect these ecosystems, 2 of 18 where a temperature increase of 1.5 to 3.5 C is projected by the end of this century [11]. This warming, together with the strong anthropogenic pressure of transformations towards agricultural and livestock uses, can alter the groundwater level, and its nutritional and biotic conditions, affecting the ecophysiology of plants [12][13][14].Vegetation in the Andes is distributed in the form of islands at the top of the mountains and is characterized by a high rate of speciation, rate of endemism, and biodiversity [15,16]. This diversity is threatened by the ascent of species from lower elevations, which could displace páramo species, reducing their distribution area, as occurs in non-tropical alpine plants [17]. ...
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Citation: Solarte, M.E.; Solarte Erazo, Y.; Ramírez Cupacán, E.; Enríquez Paz, C.; Melgarejo, L.M.; Lasso, E.; Flexas, J.; Gulias, J. Photosynthetic Abstract: Global warming and changes in land use are some of the main threats to high mountain species. Both can interact in ways not yet assessed. In this study, we evaluated the photosynthetic responses of six common páramo species within a warming experiment using open-top chambers (OTC) in conserved páramo areas with different land use histories. We did not find significant differences in the photochemical performance of the species as measured through Fv/Fm, ETR, and NPQ in response to passive warming, indicating that warmed plants are not stressed. However, NPQ values were higher in recovering areas, especially in the driest and warmest months. Leaf transpiration, stomatal conductance, and Ci were not affected by the OTC or the land use history. The photosynthetic capacity, maximum photosynthetic capacity, and carboxylation rate of RuBisCO increased in response to warming but only in the area with no anthropogenic intervention. These results suggest that species will respond differently to warming depending on the history of páramo use, and therefore not all páramo communities will respond equally to climate change. In disturbed sites with altered soil conditions, plants could have a lower breadth of physiological response to warming.
... Plant communities in the high Andes (above 3,000 m) are known as 'páramo' in the more humid areas of the northern Andes of Venezuela, Colombia, and Ecuador, and 'jalca' in northern Peru (Madriñán et al. 2013); 'puna' is found in the southern, drier Altiplano of Peru and Bolivia (Sánchez-Vega and Dillon 2006). ...
Chapter
This Report provides a comprehensive, objective, open, transparent, systematic, and rigorous scientific assessment of the state of the Amazon’s ecosystems, current trends, and their implications for the long-term well-being of the region, as well as opportunities and policy relevant options for conservation and sustainable development.
Preprint
Aim The Andean paramo is the most biodiverse high-mountain region on Earth and past glaciation dynamics during the Quaternary are greatly responsible for its plant diversification. Here, we aim at identifying potential climatic refugia since the Last Glacial Maximum (LGM) in the paramo, according to plant family, biogeographic origin, and life-form. Location The paramo region in the Northern Andes Methods We built species distribution models for 664 plant species to generate range maps under current and LGM conditions, using five General Circulation Models (GCMs). For each species and GCM, we identified potential (suitable) and potential active (likely still occupied) refugia where both current and LGM range maps overlap. We stacked and averaged the resulting refugia maps across species and GCMs to generate consensus maps for all species, plant families, biogeographic origins and life-forms. All maps were corrected for potential confounding effect due to species richness. Results We found refugia to be chiefly located in the southern and central paramos of Ecuador and Peru, especially towards the paramo ecotone with lower-elevation forests. However, we found additional specific patterns according to plant family, biogeographic origin and life-form. For instance, endemics showed refugia concentrated in the northern paramos. Main conclusions Our findings suggest that large and connected paramo areas, but also the transitional Amotape-Huancabamba zone with the Central Andes, are primordial areas for plant species refugia since the LGM. This study therefore enriches our understanding on paramo evolution and calls for future research on plant responses to future climate change.
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Aim: The Andean superpáramo ecosystem, above c. 4200 m a.s.l., currently forms an archipelago of isolated “sky islands” which provides a unique setting to study biogeography. However, there is still a poor understanding of how past geological events and climatic changes have shaped the distribution of life in this ecosystem. Our aim was to investigate the importance of biogeographic barriers in local diversifications and to analyze how populations have become isolated on current “sky islands”. Location: Neotropics, Andes, Páramo, Ecuador. Taxon: Coleoptera, Carabidae, Platynini, Dyscolus. Methods: We first used distributional data of 45 superpáramo specialist species to define areas of endemism in Ecuador. We then selected 34 isolated populations of 12 species to perform a high-throughput genome skimming approach encompassing the complete mitogenome and the complete nuclear ribosomal cluster. We also generated a time-calibrated estimation for the diversification of the group and compared it to geochronological data. Results: A high proportion (60%) of the sampled species are microendemic, restricted to a single mountain summit. Three mutually exclusive areas of endemism are limited by deep transverse valleys, in relation to Pliocene speciation events. The genome-skimming approach provides a robust phylogenetic base to analyze the diversification of species and populations throughout the Plio-Pleistocene. Main conclusions: The opening of the Interandean Valley did not play a significant role in the diversification of the group before the Pleistocene. More recently, multiple populations became isolated on the superpáramo of various volcanoes by independently colonizing it during repeated glacial-interglacial cycles. Our results highlight the joint contribution of orogeny and climatic fluctuations for explaining current distribution patterns. Each species had a different colonization history, with its populations reaching the different volcanoes at different glacial-interglacial cycles. They also provide a powerful tool to constrain the geological processes responsible for topographic changes along and across the Cordillera.
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The páramos, high-elevation Andean grasslands ranging from ca. 2800 m to the snow line, harbor one of the fastest evolving biomes worldwide since their appearance in the northern Andes 3-5 million years (Ma) ago. Hypericum (St. John's wort), with over 65% of its Neotropical species, has a center of diversity in these high Mountain ecosystems. Using nuclear rDNA internal transcribed spacer (ITS) sequences of a broad sample of New World Hypericum species we investigate phylogenetic patterns, estimate divergence times, and provide the first insights into diversification rates within the genus in the Neotropics. Two lineages appear to have independently dispersed into South America around 3.5 Ma ago, one of which has radiated in the páramos (Brathys). We find strong support for the polyphyly of section Trigynobrathys, several species of which group within Brathys, while others are found in temperate lowland South America (Trigynobrathys s.str.). All páramo species of Hypericum group in one clade. Within these páramo Hypericum species enormous phenotypic evolution has taken place (life forms from arborescent to prostrate shrubs) evidently in a short time frame. We hypothesize multiple mechanisms to be responsible for the low differentiation in the ITS region contrary to the high morphological diversity found in Hypericum in the páramos. Amongst these may be ongoing hybridization and incomplete lineage sorting, as well as the putative adaptive radiation, which can explain the contrast between phenotypic diversity and the close phylogenetic relationships.
Article
Many evolutionary studies of birds rely on the estimation of molecular divergence times and substitution rates. In order to perform such analyses, it is necessary to incorporate some form of calibration information: a known substitution rate, radiometric ages of heterochronous sequences, or inferred ages of lineage splitting events. All three of these techniques have been employed in avian molecular studies, but their usage has not been entirely satisfactory. For example, the 'traditional' avian mitochondrial substitution rate of 2% per million years is frequently adopted without acknowledgement of the associated uncertainty. Similarly, fossil and biogeographic information is almost always converted into an errorless calibration point. In both cases, the resulting estimates of divergence times and substitution rates will be artificially precise, which has a considerable impact on hypothesis testing. In addition, using such a simplistic approach to calibration discards much of the information offered by the fossil record. A number of more sophisticated calibration methods have recently been introduced, culminating in the development of probability distribution-based calibrations. In this article, I discuss the use of this new class of methods and offer guidelines for choosing a calibration technique.
Article
Abstract The biota of Hawaiian Islands is derived entirely from long distance dispersal, often followed by in situ speciation. Species descended from each colonist constitute monophyletic lineages that have diverged to varying degrees under similar spatial and temporal constraints. We partitioned the Hawaiian angiosperm flora into lineages and assessed morphological, ecological, and biogeographic characteristics to examine their relationships to variation in species number (S). Lineages with external bird dispersal (through adhesion) were significantly more species-rich than those with abiotic dispersal, but only weakly more species-rich than lineages with internal bird dispersal (involving fleshy fruits). Pollination mode and growth form (woody vs. herbaceous) had no significant effect on S, in contrast to studies of angiosperm families. S relates positively to the geographic and ecological range size of whole lineages, but negatively to local abundance and mean range sizes of constituent species. Species-rich lineages represent a large proportion of major adaptive shifts, although this appears to be an artifact of having more species. Examination of 52 sister species pairs in numerous lineages provides evidence for allopatric (including peripheral isolates) and parapatric (ecological) modes, with 15 cases of each. Although postspeciational dispersal may obscure these modes in many of the remaining cases, instances of sympatric and hybrid speciation are also discussed. Because speciation is both a consequence and a cause of ecological and biogeographic traits, speciation mode may be integral to relationships between traits. We discuss the role of speciation in shaping the regional species pool.
Article
Palynological studies in the Northern Andes have shown a gradual upheaval of the Cordillera during the Late Pliocene and the creation of the high montane environment. A long sequence of glacial and interglacial periods has been recorded from the Pleistocene. The successive appearance of new taxa, by evolutionary adaptation from the local neotropical flora and from elements immigrated from the holarctic and austral-antartic floral regions, can be followed step by step. For the Last Glacial to Holocene sequence the contemporaneity of the changes of temperature with those recorded from the northern temperate latitudes could be proved by 14 C dating During the coldest part of the Last Glacial the tree line descended to c. 2000 m altitude, i.e. 1200-1500 m lower than where it lies today. During the period from c. 21,000 to c. 13,000 B.P. the climate was, moreover much drier. Even taking the greater aridity into account, the lowering of the temperature during the coldest part of the Last Glacial may have been 6-7⚬ C or more. The lowering of the temperature in the tropical lowlands during glacial times may have been c. 3⚬ C. The temperature gradient must, therefore, have been steeper than it is today. In the coastal lowlands of Guyana and Surinam glacial-interglacial eustatic movements of sea level have been recorded. Pollen diagrams show in this area a considerable extension of savannas during glacial periods with low sea levels. In the inland savannas of the Llanos Orientales of Colombia and the Rupununi savanna of Guyana, several periods of grass-savanna and of savanna-woodland alternate during the Late Pleistocene and the Holocene; lower and higher lake levels corroborate the conclusions that these are caused by changes in the effective precipitation. One of the driest periods in the Rupununi seems to correspond to the time immediately before c. 13,000 B.P. Pollen data a series of samples from Rondonia, in the southern part of the Amazon basin, have shown that in that area grass-savannas replaced the tropical forest during a certain interval of Pleistocene age. From the above it appears that in considerable parts of the South American tropics a much drier climate prevailed during certain parts of the Pleistocene. A major dry period seems to have occurred during the later part of the Last Glacial, when the glaciers in the northern latitudes and in the Andes were reaching their maximum extension. These changes of climate and vegetation are of considerable importance for the explanation of speciation patterns and the recent distribution of plant and animal taxa.
Article
The logic of estimating the parameters in evolutive processes is considered with reference to a simple Poisson process and to the process resulting from using a counter with a non‐zero resolving time. A complete solution of the problem of estimating the parameter in a simple birth process is followed by a partial solution of the problem of estimating the two parameters in the simplest birth and death process. The same method is applied to logistic processes without, however, obtaining exact distributions.
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This introduction contains a short history of the study of the Quaternary of Colombia during the last fifteen years, and the history (and some results) of the present project, that started in 1967. The Department of Palynology of the University of Amsterdam carries out this project with grants from the Netherlands Foundation for the Advancement of Tropical Research (WOTRO), with close collaboration of other Dutch institutes and of the following Colombian institutions: Instituto Nacional de Investigaciones Geológico-Mineras (Ingeominas), Instituto de Ciencias Naturales of the Universidad Nacional (Bogotá) and the Instituto Colombiano de Antropología. A bibliography on or of interest to the Quaternary of Colombia is added.
Article
The generic circumscription and infrageneric phylogeny of Gentianella was analysed based on matK and ITS sequence variation. Our results suggested that Gentianella is polyphyletic and should be limited to species with only one nectary per petal lobe. Gentianella in such a circumscription is most closely related to one part of a highly polyphyletic Swertia. within uninectariate Gentianella two major groups could be recognized: 1) northern hemispheric species with vascularized fimbriae at the base of the corolla lobes, and 2) northern hemispheric, South American, and Austrlia/New Zealand species without vascularized fimbriae. When fimbriae are present in this latter group, they are non-vascularized. whereas ITS data suggested a sister group relationship between the fimbriate and efimbriate group, the matK data suggested paraphyly of the efimbriate group with Eurasian efimbriate species as sister to the remainder of the clade. Based on the phylogeny and using geological and fossil evidence and a molecular clock approach, it is postulated that the efimbriate lineage originated in East Asia near the end of the Tertiary. From East Asia it spread via North america to south America, and from there it reached Australia/New Zealand only once by a single long-distance dispersal event. The place of origin of the fimbriate lineage remained doubtful. The high specific diversity of Gentianella in South America probably resulted mainly from the availability of a very large alpine area open to colonization rather than from particularly high speciation rates in comparison to other taxa.