132 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
Seasonal droughts during the Miocene drove the evolution
of Capparaceae towards Neotropical seasonally dry forests
Jorge D. Mercado-Gómez1*; https://orcid.org/0000-0002-4619-0028
María E. Morales-Puentes2; https://orcid.org/0000-0002-5332-9956
Mailyn A. Gonzalez3; https://orcid.org/0000-0001-9150-5730
Julián A. Velasco4; https://orcid.org/0000-0002-2183-5758
1. Grupo Evolución y Sistemática Tropical, Departamento de Biología y Química, Universidad de Sucre, Sincelejo,
Colombia; jorge.mercado@unisucre.edu.co (*Correspondence)
2. Grupo Sistemática Biológica, Herbario UPTC, Universidad Pedagógica y Tecnológica de Colombia, Tunja, Boyacá,
Colombia; maria.morales@uptc.edu.co
3. Laboratorio de genética de la Conservación, Instituto de Investigación de Recursos Biológicos Alexander von
Humboldt, Bogotá, Colombia; magonzalez@humboldt.org.co
4. Instituto de Ciencias de la Atmósfera y Cambio Climático, Universidad Nacional Autónoma de México, Ciudad de
México, México; javelasco@atmosfera.unam.mx
Received 08-VII-2021. Corrected 28-I-2021. Accepted 21-II-2022.
ABSTRACT
Introduction: Neotropical seasonally dry forest (NSDF) climatic constraints increased endemism, and phylo-
genetic niche conservatism in species that are restricted to this biome. NSDF have a large number of endemic
Capparaceae taxa, but it is unknown if phylogenetic niche conservatism has played a role in this pattern.
Objective: We carried out an evolutionary analysis of the climatic niche of neotropical species of Capparaceae
to identify whether the climatic constraints of NSDF have played a major role throughout the family’s evolu-
tionary history.
Methods: Using three chloroplastic (ndhF, matK, rbcL) and one ribosomal (rsp3) DNA sequences, we pro-
posed a date phylogeny to reconstruct the evolutionary climatic niche dynamics of 24 Neotropical species of
Capparaceae. We tested the relationship between niche dissimilarity and phylogenetic distance between species
using the Mantel test. Likewise, we used a set of phylogenetic comparative methods (PGLS) on the phylogeny
of Capparaceae to reconstruct the main evolutionary historic events in their niche.
Results: Capparaceae originated in humid regions and subsequently, convergent evolution occurred towards
humid and dry forest during the aridification phases of the Middle Miocene (16-11 Mya). However, adaptation
towards drought stress was reflected only during the precipitation of the coldest quarter, where we found phylo-
genetic signal (Pagel λ) for gradual evolution and, therefore, evidence of phylogenetic niche conservatism. We
found convergent species-specific adaptations to both drought stress and rainfall during the Miocene, suggesting
a non-phylogenetic structure in most climatic variables.
Conclusions: Our study shows how the Miocene climate may have influenced the Capparaceae speciation
toward driest environments. Further, highlights the complexity of climatic niche dynamics in this family, and
therefore more detailed analyses are necessary in order to better understand the NSDF climatic constrictions
affected the evolution of Capparaceae.
Key words: climate; comparative methods; Miocene; niche; phylogeny.
https://doi.org/10.15517/rev.biol.trop..v70i1.47504
BOTÁNICA
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Neotropical seasonally dry forest -NSDF-
species occur from Mexico to Argentina and in
the Antilles (Banda et al., 2016). They have a
disjunct distribution that is mainly associated
with climatic conditions such as high tempera-
tures (above 25 ºC), low rainfall regimes (<
1 800 mm), and strong rainfall seasonality
(i.e., three to six months with less than 100
mm of precipitation (Banda et al., 2016).
Pennington et al. (2009) suggest that these
climatic conditions have shaped species ranges
without immigrational subsidy and, therefore,
they influence richness and patterns of ende-
mism. Furthermore, according to the same
authors climatic constraints have produced
three features (emergent from phylogenetic
studies) in taxa confined to this type of forest:
(a) endemic species are confined to a single
geographic areas (NSDF nuclei, sensu Banda
et al. (2016)), which are (b) monophyletic and
relatively old (predating the Pleistocene) and
(c) sister species often tend to inhabit the same
NSDF nuclei, suggesting phylogenetic niche
conservatism (-PNC). Phylogenetic niche con-
servatism refers to lineages that tend to retain
ancestral ecological characteristics over time
(Angulo et al., 2012; Donoghue, 2008; Pen-
nington et al., 2009).
Pennington et al. (2004) also suggested
that taxonomic groups strongly associated to
NSDF are important for understanding the
evolutionary and biogeographic history of this
biome. As suggested by floristic studies and
based on their abundance, dominance, ende-
mism, and interactions with other species,
Fabaceae, Malvaceae, Cactaceae, Zygophyl-
laceae, and Capparaceae have been suggested
to be important families in the NSDF (Banda
et al., 2016; Herazo-Vitola et al., 2017). In
particular, Neotropical Capparaceae include
around 21 genera and 106 species that toward
arid zones and tropical dry forest historically
has been related (Cornejo & Iltis, 2012; Kers,
2003; Mercado-Gómez & Escalante, 2018)
order to test the phylogenetic patterns of NSDF
proposed by (Pennington et al., 2009) found
24-endemic species of Capparaceae distributed
in five areas of endemism located in the NSDF
nuclei (Central America and northern South
America, Northern inter-Andean valleys, Cen-
tral Andean coast, Central inter-Andean val-
leys, Apurimac-Mantaro, Piedmont, Misiones
Central Brazil, and Caatinga). Furthermore,
the endemic species of Capparaceae have been
confined to NSDF nuclei and dated before
to the Pleistocene, with sister species occur-
ring in the same nucleus (Mercado-Gómez &
Escalante, 2018). These findings support two
of the three features proposed by Pennington et
al. (2009), however, whether the evolutionary
history of this family was shaped by PCN has
not been tested.
The limited geographic distribution of
Capparaceae and high endemic species in the
NSDF nuclei also suggests that species of this
family possibly originated and evolved main-
ly in these ecosystems (Mercado-Gómez &
Escalante 2018; Mercado-Gómez & Escalante,
2020). However, Mercado-Gómez and Escalan-
te (2018) also found an area of endemism locat-
ed in the humid forest of the Panama Isthmus.
In fact, Mercado-Gómez and Escalante (2020)
through track analysis, identify biogeographic
patterns related to both humid and dry forest
and, therefore, the origins and relationship of
Capparaceae with the NSDF is uncertain. In
order to improve the knowledge of the geo-
graphic and climatic relationships of Cappara-
ceae toward NSDF nuclei (Mercado-Gómez et
al., 2020), carried out a climatic affinity analy-
sis. These authors found three main climatic
associations related toward three different for-
ests dry, moist and wet. They also identified
species with broad niches that occur in both
dry, moist and wet forest (Capparidastrum
frondosum (Jacq.) Cornejo & Iltis and Crateva
tapia L.). These outcomes suggest that at first,
species of similar ecological preferences have
evolved largely independently towards moist,
wet, and dry forests throughout the evolution-
ary history of this family and then phylogenetic
climatic niche divergence (PCND) could have
occurred. Whether the ancestors of Cappara-
ceae emerged from areas climatically similar to
those of NSDF remains unknown.
134 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
In order to understand how lineages of this
family have evolved through space and time, a
climatic niche evolution analysis was carried
out to estimate the plausible ancestral climate
of the area of origin of this family and to illumi-
nate whether PNC or PCND explain the excep-
tional NSDF endemism patterns observed in
neotropical Capparaceae (Mercado-Gómez &
Escalante, 2018). Here we used a set of geo-
graphic (Broennimann et al., 2012; Warren et
al., 2008) and phylogenetic analyses (Cooper
et al., 2010; Münkemüller et al., 2015) for
24 species, in order to explain how the niche
continuum process (PNC or PCND) explains
the evolutionary history of this family. We
evaluated the macroevolutionary climatic niche
dynamics of Capparaceae to establish whether
PNC (i.e., niche stasis) or PCND have been
recurrent in the evolution of this arid climate
adapted family. We used a combination of
approaches including model-based phyloge-
netic comparative methods, numerical ecology,
and ecological niche model in order to evaluate
the climatic niche suitability of species through
temporal and spatial scales.
MATERIALS AND METHODS
Species selection, distribution, and
environmental data: A total of 24 neotropi-
cal species of Capparaceae were included in
the analyses. We assembled a comprehensive
data set of 4 700 distributional records com-
piled from several herbaria (e.g. CAUP, COL,
CUVC, FMB, HUA, ICESI, JAUM, MEDEL,
TOLI, UIS, UTMC) and online databases (e.g.
NYBG, MO, MEXU and herbaria attached
to the Species Link from SPF). All the acro-
nyms of herbaria cited follow Holmgren et al.
(1990), and an updated list is based on Thiers
(2018). Furthermore, we checked different
floras and publications (Cornejo & Iltis, 2008a;
Cornejo & Iltis, 2008b; Cornejo & Iltis, 2008c;
Cornejo & Iltis, 2008d; Cornejo & Iltis, 2009;
Cornejo & Iltis, 2010a; Cornejo & Iltis, 2010b;
Cornejo & Iltis, 2012; Cornejo et al., 2016;
Lorea-Hernández, 2004; Mercado-Gómez et
al., 2019; Mercado-Gómez & Morales-Puentes,
2020; Newman, 2007; Ruiz-Zapata, 2005;
Ruiz-Zapata, 2006). We reviewed all data for
accuracy and validity of the geographic coor-
dinates through a Geographic Information Sys-
tem (GIS; QGIS 3.4). We eliminated all dubious
localities. For all species, we removed records
repeated in multiple sources, thus retaining
only unique localities (at 1 km2 pixel). We dis-
played the geographic coordinates in decimal
degrees, based on the WGS84 datum.
In order to obtain environmental data, we
extracted climatic values from 19 variables of
WorldClim (Hijmans et al., 2005) at a spatial
resolution of 30” arc/degrees (approximately
equal to 1 km2). We overlaid the climatic
rasters on the occurrences of each species in
order to extract the climatic values for each
grid cell, resulting in a climatic data matrix
for all species. We performed a principal com-
ponent analysis (-PCA; Appendix 1A) and a
non-metric multidimensional scaling (-NMDS,
Appendix 1B) using the Pearson similarity
index to analyze collinearity among biocli-
matic variables (Dormann et al., 2013), and
we selected those that best represent the real-
ized climatic niche of Capparaceae (Appendix
1). We selected a final set of environmen-
tal variables that were revealed by the PCA
and NMDS, including: temperature seasonal-
ity (BIO4), mean temperatures of the wettest
(BIO8) and the driest (BIO9) quarters, annual
precipitation (BIO12), and precipitations of the
wettest (BIO16), the driest (BIO17), the warm-
est (BIO18) and coldest (BIO19) quarters. Part
of these variables have been defined as the
most significant NSDF and/or were used in
previous studies (Mercado-Gómez et al., 2020;
Prieto-Torres & Rojas-Soto, 2016).
Phylogeny: In order to infer a phyloge-
netic tree of Capparaceae we used 36 acces-
sions of the plastid markers ndhF, matK, rbcL,
and the mitochondrial one rsp3. From 36
accessions, we obtained 24 ingroups and 12
outgroup species to estimate the divergence
times between lineages through fossil informa-
tion and a previous dated phylogeny (Appendix
2). We aligned sequences using Atamisquea
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emarginata Miers ex Hook. & Arn., employ-
ing MUSCLE (Edgar, 2004) in Mesquite v3.1
(Diaz-Pulido & Díaz-Ruíz, 2003).
To estimate a Bayesian phylogeny, we
determined the best substitution model for
each dataset (loci) in JModelTest 2 (Darriba
et al., 2012). We selected the best model using
Akaike information criterion (AICc – Akaike,
1974). We used BEAST v2.3.0 (Bouckaert
et al., 2014) to generate the phylogenetic
estimation for all species. One cold and three
incrementally heated MCMC chains were run
for 10 000 000 generations. Settings included
2 runs and trees were sampled every 1 000
generations to minimize autocorrelation among
samples. Post analyses were carried out in
Tracer v1.7 (Rambaut et al., 2018) interpreting
likelihood values against a number of genera-
tions, an ESS > 200 for the MCM chains and
to check if the burn-in was adequately deter-
mined. Support was estimated by posterior
probabilities. In addition, TreeAnnotator v1.8.4
was used to obtain the consensus trees, exclud-
ing the first 3 000 trees. Tracer v1.7 was used
to check if chains from samples of two runs
(which yielded similar results) combined and
converged. The average standard deviation of
split frequencies between the two runs was 0.01
for all data sets. We considered nodes with PP ≥
0.90 to be well-supported.
We estimated the divergence times between
lineages using the same parameters mentioned
above for BI. We inferred a time-calibrated
phylogenetic tree through an uncorrelated
relaxed molecular clock with log-normal rate
distribution and a Yule speciation model to
estimate the times of divergence and their
credibility intervals in BEAST (Bouckaert et
al., 2014). Because Capparaceae has few fos-
sil records and has no clear taxonomic affin-
ity to current taxa, three different sources
were used to date the calibrated phylogenetic
tree: (i) We used primary calibration using
Capparis multinervis Engelhardt, dated from
the Pliocene (Berry, 1917), which has affini-
ties to Quadrella angustifolia (Kunth) Iltis &
Cornejo; (ii) We employed secondary dating
calibration data from the Cardinal-McTeague et
al. (2016) and Beilstein et al. (2010) phyloge-
netic analyses, which dated Capparaceae from
63 to 53 Mya. Furthermore (iii) we used four
fossils from sister taxa of Brassicales for node
calibrations in our molecular dating analyses,
including: fossil of Dressiantha bicarpellata
was assigned to Moringa oleifera Lam. (98.78
Mya) node (Gandolfo et al., 1998), Akania sp.,
was assigned to Akania bidwillii (Hogg) Mabb.
(61 Mya) node (Lewis & Mccourt, 2004) and
Palaeocleome lakensis (52.58 Mya) fossil was
assigned to the node Cleome sp. (Cardinal-
McTeague et al., 2016).
Niche quantification and comparison:
Given that species distribution models must
consider historical factors affecting the geo-
graphical distributions, we created an area for
each species (or M sensu BAM diagram; see,
(Soberon & Peterson, 2005) based on occur-
rence points and the intersection with terrestrial
ecoregions (Olson et al., 2001) and biogeo-
graphical provinces (Morrone, 2014). We used
these areas (M) to clip the climatic variables
chosen for each species and to perform the
niche similitude test using the environmental
principal component analysis (PCA-env) pro-
posed by Broennimann et al. (2012) in the Eco-
spat R package (Di Cola et al., 2016). We used
the two first axes of the PCA-env calibrated on
the entire environmental space of the species
distribution area “M” to obtain the species
climatic space through a grid of 100 x 100 cells
in which each cell corresponded to a unique
vector for the available environmental condi-
tions in the study area (Broennimann et al.,
2012). We utilized this information to estimate
the similarity between the niches occupied
by the species studied through Schoener’s D
(Freshwater et al., 1994), implemented in the
ENMTools R package (Warren et al., 2008).
Niche evolution analyses: To explore the
relationships between climatic niche diver-
gence and phylogenetic distances (maximum
clade credibility tree) we used a Mantel test
based on dissimilarity matrices. We employed
the matrix of niche similitude from Schoener’s
136 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
D metric outcomes and patristic distances cal-
culated from PATRISTIC (Fourment & Gibbs,
2006) from our phylogenetic estimation. The
Mantel test was run in the ade4 Package R
(Bougeard & Dray, 2018).
We calculated the mean value of those
selected climatic variables for each species and
estimated the phylogenetic scaling parameters
λ, κ and δ (Pagel, 2002) using the time-cali-
brated phylogenetic tree. All these parameters
range from 0 to 1. When l takes values of 0 it
indicates phylogenetic signal absence, while a
λ near 1 shows a phylogenetic signal accord-
ing to Brownian motion (Hernández et al.,
2013). When κ takes values of 1, trait evolu-
tion is directly proportional to branch length;
therefore, slow evolution is better supported
(Hernández et al., 2013), whereas a κ near 0
indicates that character change is independent
of evolutionary rate with rapid change during
speciation or immediately following it suggest-
ed as is expected from punctuated equilibrium.
Likewise, δ near 1 indicates gradual evolution.
When δ is near 0, it indicates earlier trait evolu-
tion or ‘early burst’, it is indicative of adaptive
radiation, while δ near 1 indicates later trait
evolution, suggesting species specific adapta-
tion (Hernández et al., 2013; Pagel, 2002). We
investigated the mode of evolution along with
each climatic niche component, fitting five
alternative models of evolution: (1) A Brown-
ian Motion (BM), (2) Ornstein–Uhlenbeck
(OU), (3) Early Burst (EB), (4) White Noise
(WN), and (5) Drift Models (DF). We chose
the best-fit model using the AIC corrected for
a small sample size (AICc). We carried out all
evolutionary analyses in the Geiger package on
R (Harmon et al., 2008).
We also mapped the climatic variables with
a phylogenetic signal on the phylogeny through
ancestral state reconstructions under maximum
likelihood estimation, using Phytools 0.3-93
package on R (Revell, 2012). Furthermore, we
generated traitgrams climatic variables with
phylogenetic signal to explore the evolution-
ary trajectories of climatic niche through time.
In order to assess if PCND could help explain
the evolution of neotropical Capparaceae, we
evaluated whether niche convergence was a
recurrent pattern throughout Capparaceae evo-
lution in dry and humid places using the SUR-
FACE R package (Ingram & Mahler, 2013).
RESULTS
Phylogeny: The Bayesian tree, based on
mitochondria and chloroplastic sequences, we
obtain the phylogenetic hypotheses for Neo-
tropical species of Capparaceae. Capparaceae
its monophyletic and includes at least two main
linages, Crateva and all Neotropical species
(Fig. 1). Our outcomes also show that Cynoph-
alla and Quadrella to be monophyletic groups,
and Capparidastrum and Crateva paraphyletic.
Likewise, we also found that sister lineages of
the neotropical species inhabited Africa and
Australasia and that Crateva was the sister
clade of the rest of Capparaceae. The median
age divergence for neotropical lineages was
23.3 Mya and for the Crateva clade, 9.54 Mya
(Fig. 2).
Niche quantification and comparison:
According Mantel test, the values of observa-
tion (0.91) of the Pearson correlation between
the niche overlap index (D) and phylogenetic
distance matrices and the p-value = 0.94 indi-
cate that our observed matrix correlation has
not difference or is similar to those obtained
from that resulting of a random process of
scrambling the rows and column of the two
matrices and, therefore, show a strong positive
correlation between climatic niche and phy-
logeny indicating that phylogenetically more
closely related species have more similar nich-
es than species more distantly related.
The PCA-env returned two axes that
together explained 72 % of the data variation,
where PC1 explained 56 % and PC2 16 %.
The former explained the bioclimatic vari-
ables of precipitation (BIO12, BIO16, BIO17,
BIO18, and BIO19), while the latter explained
the temperature (BIO4, BIO 8, and BIO9).
Precipitation variables were the most impor-
tant bioclimatic variables (Appendix 3). The
hypotheses of niche similarity in almost all
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paired comparison between neotropical Cap-
paraceae species were accepted (p ≤ 0.05, Table
1). In Quadrella, the niche similarity analysis
showed statistically significantly niche overlap
under the (Warren et al., 2008) null model (e.g.
Q. cynophallophora-Q. angustifolia, D = 0.26;
Q. cynophallophora-Q. indica D = 0.44; Q.
cynophallophora-Q. odoratissima, D = 0.48).
Similarly, we also found significant niche over-
lap between several genera (Morisonia-Cappa-
ricordis D = 0.68; Atamisquea-Neocapparis D
= 0.24; Colicodendron - Quadrella D = 0.68).
Furthermore, the climatic niche of Preslianthus
pittieri (Standl.) Iltis & Cornejo was not similar
to other species, while the climatic niche of
Atamisquea emarginata Miers ex Hook. & Arn.
was similar to three species (p ≥ 0.05; Table
1). Conversely, Capparicordis crotonoides
(Kunth) Iltis & Cornejo, Colicodendron scabri-
dum (Kunth) Seem, Cynophalla hastata (Jacq.)
J. Presl, and Cynophalla flexuosa (L.) J. Presl
showed that their climatic niches were more
similar than expected by chance (Table 1).
Niche evolution analyses: We found that
temperature seasonality (BIO4), mean tem-
peratures of wettest (BIO8) and driest (BIO9)
quarters, annual precipitation (BIO12), and
precipitations of the wettest (BIO16), the dri-
est (BIO17), the warmest (BIO18) and coldest
(BIO19) quarters, have phylogenetic indepen-
dence (λ near to 0) or low phylogenetic signals.
According to the mode of evolution (κ), all cli-
matic variables analyzed here, excluding pre-
cipitation during the coldest quarter (BIO19),
indicated proportionally more evolutionary
Fig. 1. Bayesian maximum clade credibility phylogenetic tree for Capparaceae based from cpDNA (ndhF, matK, rbcL) and
mtDNA (rps3) sequence data. Bayesian posterior probabilities (PP) values are indicated next to the nodes.
138 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
change in shorter branches and, therefore, sug-
gesting punctuated equilibrium (κ = 0). In addi-
tion, we found that longer paths contributed
more to the evolution of climatic variables that
represent the realized niche of the Capparaceae
(δ = 1) and, hence, species-specific adaptation
has been dominant throughout the evolutionary
history of this family. However, strong phylo-
genetic signal (λ = 1) and gradual evolution
(κ = 1) were found in the precipitation of the
coldest quarter (BIO19). The WN evolutionary
model had a better fit in BIO4, BIO8, BIO9,
BIO12, BIO16, BIO 17 and BIO18, while BM
had a better fit in BIO19 (Table 2).
The ancestral climatic niche reconstruc-
tion for the precipitation of the coldest quarter
(which had a strong phylogenetic signal) was
represented by a color gradient over a simpli-
fied phylogenetic tree (Fig. 3A). This suggests
that the most recent common ancestor (MRCA)
of the Neotropical Capparaceae evolved toward
seasonal drought during coldest periods. We
found that the MRCA of Crateva was inferred
to have occupied sites with medium values of
Fig. 2. Time calibrated bayesian maximum clade credibility phylogenetic tree for Capparaceae based from cpDNA (ndhF,
matK, rbcL) and mtDNA (rps3) sequence data and five fossil calibrations. The values to the right of each node, indicate
mean divergence times with the bar representing the 95 % highest posterior density intervals. The red nodes (C) represent
the fossil (primary) and secondary calibrated nodes.
139
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TABLE 1
Niche similarities of the studied taxa based on the Schoener’s D Asterisks (*) indicate significant results (P < 0.05).
D/I Anisocapparis
speciosa
Atamisquea
emarginata
Belencita
nemorosa
Calanthea
stenosepala
Capparicordis
crotonoides
Capparidastrum
frondosum
Colicodendron
scabridum
Crateva
palmeri
Crateva
tapia
Cynophalla
amplissima
Cynophalla
flexuosa
Cynophalla
hastata
Atamisquea emarginata 0.38
Belencita nemorosa 0.30 0.00
Calanthea stenosepala 0.22 0.00 0.42
Capparicordis crotonoides 0.59 0.38 0.49 0.033
Capparidastrum frondosum 0.13 0.16 0.52 0.22 0.45
Colicodendron scabridum 0.58 0.20 0.49 0.09 0.63 0.72
Crateva palmeri 0.35 0.12 0.48 0.19 0.70 0.72 0.43
Crateva tapia 0.10 0.18 0.42 0.23 0.44 0.81 0.28 0.61
Cynophalla amplissima 0.06 0.02 0.096 0.08 0.39 0.55 0.49 0.47 0.22
Cynophalla flexuosa 0.52 0.22 0.48 0.19 0.68 0.48 0.62 0.36 0.82 0.46
Cynophalla hastata 0.48 0.33 0.40 0.17 0.61 0.42 0.47 0.42 0.51 0.17 0.50
Cynophalla retusa 0.40 0.29 0.27 0.00 0.61 0.28 0.62 0.40 0.39 0.16 0.55 0.46
Cynophalla sessilis 0.29 0.03 0.75 0.32 0.53 0.60 0.38 0.45 0.30 0.32 0.52 0.54
Cynophalla verrucosa 0.21 2.22 0.60 0.17 0.64 0.52 0.49 0.50 0.43 0.28 0.48 0.57
Monilicarpa tenuisiliqua 0.21 0.02 0.57 0.19 0.64 0.52 0.47 0.52 0.61 0.52 0.53 0.54
Morisonia americana 0.36 0.06 0.74 0.18 0.68 0.78 0.61 0.32 0.64 0.53 0.78 0.68
Neocapparis pachaca 0.24 0.00 0.76 0.30 0.72 0.61 0.51 0.10 0.56 0.36 0.41 0.55
Preslianthus pittieri 0.01 0.00 0.037 0.00 0.005 0.19 0.027 0.54 0.12 0.10 0.12 0.016
Quadrella angustifolia 0.00 0.01 0.36 0.00 0.46 0.10 0.022 0.52 0.34 0.15 0.29 0.44
Quadrella cynophallophora 0.38 0.17 0.31 0.37 0.63 0.40 0.39 0.54 0.32 0.20 0.51 0.57
Quadrella indica 0.36 0.01 0.62 0.29 0.55 0.40 0.64 0.52 0.68 0.73 0.68 0.63
Quadrella odoratissima 0.38 0.18 0.45 0.22 0.67 0.75 0.58 0.35 0.64 0.42 0.47 0.54
Steriphoma paradoxum 0.44 0.34 0.24 0.006 0.38 0.47 0.42 0.55 0.40 0.17 0.28 0.25
140 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
TABLE 1 (Continued)
Niche similarities of the studied taxa based on the Schoener’s D Asterisks (*) indicate significant results (P < 0.05).
D/I Cynophalla
retusa
Cynophalla
sessilis
Cynophalla
verrucosa
Monilicarpa
tenuisiliqua
Morisonia
americana
Neocapparis
pachaca
Preslianthus
pittieri
Quadrella
angustifolia
Quadrella
cynophallophora
Quadrella
indica
Quadrella
odoratissima
Atamisquea emarginata
Belencita nemorosa
Calanthea stenosepala
Capparicordis crotonoides
Capparidastrum frondosum
Colicodendron scabridum
Crateva palmeri
Crateva tapia
Cynophalla amplissima
Cynophalla flexuosa
Cynophalla hastata
Cynophalla retusa
Cynophalla sessilis 0.13
Cynophalla verrucosa 0.11 0.75
Monilicarpa tenuisiliqua 0.24 0.58 0.82
Morisonia americana 0.49 0.56 0.53 0.50
Neocapparis pachaca 0.06 0.67 0.76 0.50 0.35
Preslianthus pittieri 0.065 0.10 0.11 0.16 0.18 0.02
Quadrella angustifolia 0.029 0.27 0.35 0.22 0.53 0.33 0.00
Quadrella cynophallophora 0.55 0.42 0.47 0.55 0.51 0.40 0.018 0.26
Quadrella indica 0.31 0.50 0.70 0.67 0.84 0.77 0.15 0.44 0.53
Quadrella odoratissima 0.22 0.41 0.47 0.66 0.82 0.64 0.08 0.48 0.55 0.54
Steriphoma paradoxum 0.090 0.18 0.48 0.62 0.46 0.38 0.22 0.10 0.24 0.50 0.48
141
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precipitation during the coldest quarter (Fig.
3A) at around 500 mm. Further, the MRCA
of the other Neotropical species evolved from
places with humidity around 300 mm during
seasonal drought periods, occurring in both
humid and dry forest. P. pittieri and C. frondo-
sum evolved towards more humid places, but
their MRCA occurred in drier areas. According
to our results, the MRCA of P. pittieri inhabited
drier places but then one clade evolved towards
humid areas and another towards dry forests,
including the clades Quadrella, Morisonia,
Calanthea and Capparicordis (Fig. 3A).
According to the phyloclimatic reconstruc-
tion (Fig. 3B), we found that the Neotropical
species of Capparaceae shifted towards humid
and dry areas independently in several lin-
eages. It is noteworthy that ancestral character
reconstructions clearly show that all Neotropi-
cal clades had a more pronounced evolution
of climatic niches closer to the present time,
particularly in the last 10 Mya. These outcomes
are supported by the convergent evolutionary
analysis (Fig. 4A, Fig. 4B) that revealed two
climatic regimes: niche convergence towards
dry (C. scabridum and A. emarginata ancestor)
TABLE 2
Outcomes of λ, κ and δ parameters and AICc for evolutionary models
Models BIO4 BIO8 BIO9 BIO12 BIO16 BIO17 BIO18 BIO19
Lambda 1.68E-144 2.39E-112 2.88E-203 2.37E-203 5.58E-89 3.46E-132 3.79E-181 1*
Kappa 2.04E-187 1.98E-179 1.66E-171 1.06E-136 9.40E-02 6.74E-201 1*
Delta 2.9 2.9 2.9 2.9 2.9 2.9 2.9 1.59*
BM 318.49 171.78 128.86 456.83 397.05 365.63 391.13 318.92*
OU 294.34 144.05 108.04 444.59 380.66 354.29 369.53 320.87
EB 321.12 174.41 131.49 459.46 399.68 368.26 393.76 321.55
WN 291.69* 141.40* 105.40* 442.08* 378.26* 353.36* 366.90* 330.28
Drift 321.12 174.41 131.49 459.46 399.68 368.26 393.76 321.55
Brownian Motion (BM), Ornstein–Uhlenbeck (OU), Early Burst (EB), White Noise (WN) and Drift Models (DF). Asterisks
(*) indicate the best fits models.
Fig. 3. Ancestral reconstructions for precipitation of coldest quarter, BIO19. A. Ancestral character reconstructions. Colours
of branches reflect values of climatic variables scores estimated by maximum likelihood on the MCCT. B. Ancestral state
reconstructions. X-axis represents divergence times (Mya) and the y-axis represents the reconstructed mean character values.
142 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
and niche convergence towards humid environ-
ments (P. pittieri ancestor) (Fig. 3B). Similarly,
evolutionary rates were higher for precipitation
(73 983.96) than they were for temperature
(15.09) across the evolution of the species
analyzed here.
DISCUSSION
The results of this study provide a com-
prehensive view of how some species of Cap-
paraceae evolved through the climatic space
through their evolutionary history. We evalu-
ated relationships between climatic niche
attributes and phylogenetic relationships with
the aim of establishing the climatic niche
dynamics of this family when colonizing dry
forested areas in the Neotropics. We found
some broad climatic affinities (niche overlap)
among Capparaceae species using a multivari-
ate analysis of climatic variables. Besides we
found niche overlap within Quadrella spe-
cies and between Morisonia-Capparicordis,
Atamisquea-Neocapparis and Colicodendron-
Quadrella we also found significant relation-
ships between the climatic niche overlap index
(D) and phylogenetic distance (Mantel test; P =
0.94). However, this latter outcome was found
at genus level.
Although we did not find a strong phylo-
genetic signal in most climatic variables herein
analyzed and apparently PCND seems likely to
play a major role in the evolution of Cappara-
ceae, we found that precipitation of the coldest
quarter (BIO19) had a strong phylogenetic
signal (λ), and a slow (κ) and gradual evolu-
tion (δ) were better supported, while Brownian
Motion was the best fitted evolutionary model.
According to Crisp and Cook (2012) and
Fig. 4. Convergent evolution of climatic niche in Neotropical Capparaceae using a SURFACE approach. A. Calibrated
phylogeny for Neotropical Capparaceae species with climatic niche data and adaptive regimes identified. Coloured branches
represent convergent adaptive peaks (or climate regimes) and grey or black branches represent non-convergent regimes.
B. Climatic space occupied by species analyzed, large points represent the same convergent adaptive regimes identified in
the phylogeny and small points represent the species that have evolved around these adaptive optima. Red points represent
convergent regimes toward dry forest, while grey point to humid forest.
143
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
Münkemüller et al. (2015) these results could
be considered as consistent with a scenario
of PNC for adaptations to precipitation of the
coldest periods. Coldest periods mainly include
the months December, January, February, and
March. Although the frequency and intensity
of seasonal drought depends largely upon lati-
tudinal position (Arango et al., 2021), with the
shortest and least severe dry periods found on
or within few degrees of the equator (Murphy &
Lugo, 1986), it is clear that all NSDF fragments
have a prominent dry period during the coldest
months (Gentry, 1995), which could even drive
the phylogenetic information into communi-
ties along latitudinal gradients (Arango et al.,
2021). Drought stress tolerance is one the most
important adaptations of NSDF species to resist
seasonal long-term drought (Engelbrecht &
Kursar, 2003). The latter can be defined as the
ability of species to survive desiccation while
minimizing reductions in growth and fitness
(Engelbrecht & Kursar, 2003). We suggest
that colonization of Capparaceae to new dry
areas occurred via environmental filtering that
produced phylogenetic niche conservatism of
those traits related to drought stress. This pat-
tern has been found in other clades of dry forest
(Angulo et al., 2012; De-Nova et al., 2012).
Likewise, we found that the realized niche
evolution of Capparaceae was more concentrat-
ed in derived phylogenetic branches (e.g. recent
evolutionary influence traits) than in deep phy-
logenetic splits (Cooper et al., 2010) and, there-
fore, that lability was intimately connected to
their expansion into new climate space at least
10 Mya (Fig. 3A) ago and the more recent
evolution toward the dry and humid forest.
Neotropical species of this family evolved from
ancestors that inhabited humid sites, where
e.g. Crateva, the sister clade of all neotropi-
cal species inherited this condition from their
ancestors and currently occurs at humid sites
(Mercado-Gómez et al., 2020). However, dur-
ing the Middle Miocene species-specific adap-
tations to drier sites also occurred throughout
an arid period, which was further enhanced by
a global cooling phase that resulted in polar ice
sheets with the addition of concomitant local
volcanism might have enhanced rain shadows
due to temperature drop (Churchill & Lin-
ares, 1995; Hernández-Hernández et al., 2013;
Hernández-Hernández et al., 2014).
Moore and Robertson (2014) suggested
that ecological opportunities emerged starting
from long-distance dispersal events, when an
alien lineage took advantage of an array of
newly formed or previously unfilled niches
and particularly when a change in the envi-
ronment made new resources available. This
would have created new challenges or opened
new environmental niches (Tan et al., 2016).
Within the Miocene and Pliocene, new niches
emerged from the cooler/drier conditions that
produced drought-stress, and this presented
strong selective pressures on lineages to evolve
and successfully survive and reproduce in these
new environments (Hernández-Hernández et
al., 2014). Niche availability, understood as
an ecological opportunity (Michel et al., 2013;
Stroud & Losos, 2016), also may affect the
species diversification dynamics and therefore
plays an important role in species evolution
(Paun et al., 2016). It is very likely that species
of Capparaceae might have responded to Mio-
cene aridification adapting to the drier condi-
tions that emerged as a novel ecological space
(Hernández-Hernández et al., 2014).
We detected convergent and asychronical-
ly evolution in Capparaceae to dry places dur-
ing the driest periods of the Miocene (Churchill
& Linares, 1995; Hernández-Hernández et al.,
2013; Hernández-Hernández et al., 2014) in B.
nemorosa (23 Mya), Neocapparis-Atamisquea
(18 Mya), Monilicarpa-Anisocapparis (16
Mya), Calanthea-Morisonia-Capparicordis
(14 Mya), Colicodendron (12 Mya) and Cyno-
phalla (11 Mya). Our results were consistent
with those found by De-Nova et al. (2012)
in Burseraceae, who find that during these
arid periods, species of this family adapted
and expanded their distributions from Mexico
to South America. Furthermore, Willis et al.
(2014) also found similar results in the Mal-
phigiaceae, and Hernández-Hernández et al.
(2014) suggested that the radiation of the Cac-
taceae coincided with the expansion of aridity
144 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
in North America during the late Miocene. An
increase of diversification during these arid
periods is also consistent with the NSDF that
arose in North America during the middle
Eocene and expanded in distribution south-
wards towards Central and South America
throughout the Miocene and have persisted for
19 Ma hosting endemic species that exhibiting
strong phylogenetic niche conservatism (Lavin,
2006; Pennington et al., 2004; Pennington et
al., 2009; Särkinen et al., 2012).
Although we found evidence of PNC in
the precipitation of the coolest quarter variable
(BIO19), an overall climatic differentiation
and convergent evolution was found in both,
species adapted to dry and species adapted to
humid forests. Ecological convergent evolution
was found at least two clades (Atamisquea –
Cynophalla and Colicodendron – Quadrella),
such clade-wide convergence can be inter-
preted as lineages independently responding
to the same selective regimes, or equivalently,
discovering the same adaptive peaks on a mac-
roevolutionary adaptive landscape (Ingram &
Mahler, 2013), suggesting that niche conserva-
tism has not played the major role in the early
evolution of the Neotropical species of this
family. Our outcomes show that PNC possibly
played a major role during the late evolution
of the group, where it can be detected in some
clades like Cynophalla and Quadrella mainly.
Angulo (2012), found in Barkeria, that this
clade shows PNC to dry forest since the middle
Pliocene to the Pleistocene. However, our
phylogenetic bias (only 24 of species included
in the phylogeny) does not allow us to better
understand the evolution of Neotropical Cappa-
raceae and therefore more analyses are neces-
sary to improve the knowledge of the climatic
history of this important dry forest family.
Our results also support that high het-
erogeneity and patchy distribution of habitat
resulting from climatic changes during the
Miocene have allowed convergent evolution
towards humid sites in Capparidastrum and
Preslianthus (Fig. 3A, Fig. 3B). Nevertheless,
this evolution occurred independently multiple
times. Preslianthus (e.g. evolved into humid
places during the middle Miocene) but C.
frondosum evolved into humid sites later in the
Pliocene. However, our outcomes also showed
that their MRCA (Fig. 3B) was adapted to dry
areas. Mercado-Gómez et al. (2020) found that
C. frondosum and C. tapia have larger climatic
variations correlated with greater distribution
areas for species, a correlation known as niche
breadth. Niche breadth explains why these spe-
cies are tolerant to dry and moist environments
along the transitional areas between ecosystem
(Sexton et al., 2017).
Analyzing climatic niche evolution among
species of Capparaceae based on environ-
mental data and phylogenetic information, we
found that the Neotropical species of this fam-
ily may have emerged from the Middle Mio-
cene, where its ancestor inhabited humid sites.
We also found that during the driest periods
of the Miocene, both divergent and conver-
gent evolution occurred, resulting in two main
groups associated with dry and humid forests.
Our analysis recovered the evolutionary
history of the climatic niche of the Capparaceae
toward humid and dry places. Furthermore,
taxa constrained by NSDF also show conver-
gent evolution more than phylogenetic niche
conservatism. However, due to our sparse
phylogenetic sampling (24 species from 104),
our findings only allow us to suggest that
Cynophalla and Quadrella are the only taxa
that might provide robust inferences about
the NSDF flora evolution. We suggest more
detailed phylogenetic analyses including more
Neotropical taxa and additional morphological
data such as leaves or woody traits in order
to search for additional evidence that might
improve our knowledge on the evolutionary
history of NSDF and the evolution of Cappara-
ceae in this biome.
Ethical statement: the authors declare
that they all agree with this publication and
made significant contributions; that there is no
conflict of interest of any kind; and that we fol-
lowed all pertinent ethical and legal procedures
and requirements. All financial sources are
fully and clearly stated in the acknowledgments
145
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
section. A signed document has been filed in
the journal archives.
See Digital Appendix - a10v70n1-s1-Digital
appendix
ACKNOWLEDGMENTS
The first author acknowledges the doctoral
scholarships 647 of COLCIENCIAS and “Uni-
versidad de Sucre” for the financial support
of his doctoral studies. In addition, we thank
Thomas Defler and Richard Abbott for its
commentaries to the manuscript and English
revision.
RESUMEN
Las sequías estacionales del Mioceno impulsaron
la evolución de Capparaceae hacia los bosques
neotropicales estacionalmente secos
Introducción: Las limitaciones climáticas del bosque neo-
tropical estacionalmente seco (NSDF) produjeron endemis-
mo y conservadurismo filogenético del nicho en especies
restringidas a este bosque. En las Caparáceas neotropicales
se ha encontrado endemismo en los NSDF, pero se des-
conoce si el conservadurismo de nicho filogenético ha
influido en su evolución.
Objetivos: Se llevó a cabo un análisis evolutivo del nicho
climático de las especies neotropicales de Capparaceae
para evaluar si las limitaciones climáticas del bosque neo-
tropical estacionalmente seco (NSDF) han jugado un papel
importante a lo largo de la historia evolutiva de la familia.
Métodos: Usando tres secuencias de ADN cloroplastico
(ndhF, matK, rbcL) y una ribosomal (rsp3) se propuso una
filogenia datada para reconstruir la dinámica evolutiva del
nicho climático de 24 especies Neotropicales de Cappara-
ceae. Utilizando la prueba de Mantel, se realizaron análisis
para establecer si hay diferencia de nicho y la distancia
filogenética entre especies. Asimismo, se emplearon un
conjunto de métodos comparativos filogenéticos sobre
la filogenia de la familia para reconstruir los principales
eventos históricos evolutivos en su nicho.
Resultados: Capparaceae se originó en regiones húmedas
y posteriormente se dio una evolución convergente hacia
bosque húmedo y seco durante las fases de aridificación del
Mioceno Medio (16-11 Ma). Sin embargo, la adaptación al
estrés por sequía se reflejó solo en la precipitación del cuar-
to más frío del año, donde se evidencio señal filogenética,
evolución gradual y, por lo tanto, evidencia de conservadu-
rismo de nicho filogenético. También se hallaron especies
con adaptaciones convergentes específicas tanto al estrés
por sequía como a las lluvias durante el Mioceno, sugirien-
do la carencia de estructura filogenética en la mayoría de
las variables climáticas.
Conclusiones: Este estudio muestra cómo el clima del
Mioceno pudo haber influenciado la especiación de Cappa-
raceae hacia ambientes mas secos. Además, la compleja
dinámica del nicho climático en esta familia y, por lo
tanto, la necesidad de realizar análisis más detallados para
comprender mejor como las constricciones climáticas del
NSDF afectaron la evolución de Capparaceae.
Palabras clave: clima; métodos comparativos; mioceno;
nicho; filogenia.
REFERENCES
Angulo, D. F., Ruiz-Sanchez, E., & Sosa, V. (2012). Niche
conservatism in the Mesoamerican seasonal tropical
dry forest orchid Barkeria (Orchidaceae). Evolutio-
nary Ecology, 26, 991–1010.
Arango, A., Villalobos, F., Prieto-Torres, D. A., & Guevara,
R. (2021). The phylogenetic diversity and structure of
the seasonally dry forests in the Neotropics. Journal
of Biogeography, 48(1), 176–186.
Banda, K., Delgado-Salinas, A., Dexter, K. G., Linares-
Palomino, R., Oliveira-Filho, A., Prado, D., Pullan,
M., Quintana, C., Riina, R., Rodríguez, G. M., Wein-
tritt, J., Acevedo-Rodríguez, P., Adarve, J., Álvarez,
E., Aranguren, A., Arteaga, J. C., Aymard, G., Cas-
taño, A., Ceballos-Mago, N., … Pennington, R. T.
(2016). Plant diversity patterns in neotropical dry
forests and their conservation implications. Science,
353(6306), 1383–1387.
Beilstein, M. A., Nagalingum, N. S., Clements, M. D.,
Manchester, S. R., & Mathews, S. (2010). Dated
molecular phylogenies indicate a Miocene origin for
Arabidopsis thaliana. Proceedings of the National
Academy of Sciences, 107(43), 18724–18728.
Berry, E. W. (1917). Fossil plants from Bolivia and
their bearing upon the age of the uplift of the Eas-
tern Andes. Proceedings of United States National
Museum, 54(2229), 103–164.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.
H., Xie, D., Suchard, M. A., Rambaut, A., & Drum-
mond, A. J. (2014). BEAST 2: A Software Platform
for Bayesian Evolutionary Analysis. PLOS Computa-
tional Biology, 10(4), e1003537.
Bougeard, S., & Dray, S. (2018). Supervised Multiblock
Analysis in R with the ade4 Package. Journal of
Statistical Software, 86(1), 1–17.
Broennimann, O., Fitzpatrick, M. C., Pearman, P. B.,
Petitpierre, B., Pellissier, L., Yoccoz, N. G., Thuiller,
W., Fortin, M. J., Randin, C., Zimmermann, N. E.,
Graham, C. H., & Guisan, A. (2012). Measuring
146 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
ecological niche overlap from occurrence and spatial
environmental data. Global Ecology and Biogeogra-
phy, 21(4), 481–497.
Cardinal-McTeague, W. M., Sytsma, K. J., & Hall, J. C.
(2016). Biogeography and diversification of Brassi-
cales: A 103 million year tale. Molecular Phylogene-
tics and Evolution, 99, 204–224.
Churchill, S., & Linares, E. (1995). Prodromus bryologiae
novo-granatensis. Introduccion a la Flora de Mus-
gos de Colombia. Biblioteca José Jerónimo Triana,
Colombia.
Cooper, N., Jetz, W., & Freckleton, R. P. (2010). Phyloge-
netic comparative approaches for studying niche con-
servatism. Journal of Evolutionary Biology, 23(12),
2529–2539.
Cornejo, X., & Iltis, H. (2008a). The reinstatement of
Beautempsia (Capparaceae) and a key to the genera
of neotropical Capparaceae with variously stellate or
peltate indumenta. Journal of the Botanical Research
Institute of Texas, 3(2), 683–689.
Cornejo, X., & Iltis, H. H. (2008b). The reinstatement of
Capparidastrum (Capparaceae). Harvard Papers in
Botany, 13(2), 229–236.
Cornejo, X., & Iltis, H. H. (2008c). A revision of the Ame-
rican species of the genus Crateva (Capparaceae).
Harvard Papers in Botany, 13(1), 121–135.
Cornejo, X., & Iltis, H. H. (2008d). A revision of Coli-
codendron (Capparaceae). Journal of the Botanical
Research Institute of Texas, 2(1), 75–93.
Cornejo, X., & Iltis, H. H. (2010a). Studies in Capparaceae
XXVII: Six new taxa and new combination in Qua-
drella. Journal of the Botanical Research Institute of
Texas, 4(1), 75–91.
Cornejo, X., & Iltis, H. H. (2010b). Lectotypification and
a new combination in Cynophalla (Capparaceae).
Rodriguésia, 61(1), 153–155.
Cornejo, X., & Iltis, H. H. (2012). Capparaceae. In S. Car-
vajal, & L. M. Gonzalles- Villareal (Eds.), La flora de
Jalisto y Areas colindantes (pp. 1–71). Universidad
de Guadalajara, México.
Cornejo, X., & Iltis, H. H. (2009). Hispaniolanthus: A new
genus of Capparaceae endemic to Hispaniola. Har-
vard Papers in Botany, 14(1), 9–14.
Cornejo, X., Maciel, J. R., Marques, J. S., Neto, R. L. S.,
& Costa-e-Silva, M. B. (2016). Capparaceae in Lista
de Espécies da Flora do Brasil. Jardim Botânico do
Rio de Janeiro, Brasil.
Crisp, M. D., & Cook, L. G. (2012). Phylogenetic niche
conservatism: what are the underlying evolutionary
and ecological causes? New Phytologist, 196(3),
681–694.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D.
(2012). jModelTest 2: more models, new heuris-
tics and parallel computing. Nature Methods, 9(8),
772–772.
De-Nova, J. A., Medina, R., Montero, J. C., Weeks, A.,
Rosell, J. A., Olson, M. E., Eguiarte, L. E., & Maga-
llón, S. (2012). Insights into the historical construc-
tion of species-rich Mesoamerican seasonally dry
tropical forests: the diversification of Bursera (Burse-
raceae, Sapindales). New Phytologist, 193, 276–287.
Di Cola, V., Broennimann, O., Petitpierre, B., Breiner
Frank, T., D’Amen, M., Randin, C., Engler, R.,
Pottier, J., Pio, D., Dubuis, A., Pellissier, L., Mateo
Rubén, G., Hordijk, W., Salamin, N., & Guisan, A.
(2016). ecospat: an R package to support spatial
analyses and modeling of species niches and distri-
butions. Ecography, 40(6), 774–787.
Diaz-Pulido, G., & Díaz-Ruíz, M. (2003). Diversity of
benthic marine algae of the Colombian Atlantic.
Biota Colombiana, 4(2), 203–246.
Donoghue, M. (2008). A Phylogenetic perspective on the
distribution of plant diversity. In J. Avise, S. Hubbell,
& F. Ayala (Eds.). In the Light of Evolution, Volume
II: Biodiversity and Extinction (pp. 247–266). Natio-
nal Academies Press.
Dormann, C. F., Elith, J., Bacher, S., Buchmann, C.,
Carl, G., Carré, G., García Marquez, J., Gruber,
B., Lafourcade, B., Leitão, P., Münkemüller, T.,
McClean, C., Osborne, P., Reineking, B., Schrö-
der, B., Skidmore, A., Zurell, D., & Lautenbach,
S. (2013). Collinearity: a review of methods to
deal with it and a simulation study evaluating their
performance. Ecography, 36(1), 27–46. https://doi.
org/10.1111/j.1600-0587.2012.07348.x
Edgar, R. (2004). MUSCLE: multiple sequence alignment
with high accuracy and high throughput. Nucleic
Acids Research, 32(5), 1792–1797.
Engelbrecht, B. M. J., & Kursar, T. A. (2003). Comparative
drought-resistance of seedlings of 28 species of co-
occurring tropical woody plants. Oecologia, 136(3),
383–393.
Fourment, M., & Gibbs, M. J. (2006). PATRISTIC: a pro-
gram for calculating patristic distances and graphi-
cally comparing the components of genetic change.
BMC Evolutionary Biology, 6(1), 1.
Freshwater, D. W., Fredericq, S., Butler, B. S., Hom-
mersand, M. H., & Chase, M. W. (1994). A gene
phylogeny of the red algae (Rhodophyta) based on
plastid rbcL. Proceedings of the National Academy of
Sciences, 91(15), 7281–7285.
Gandolfo, M. A., Nixon, K. C., & Crepet, W. L. (1998). A
new fossil flower from the Turonian of New Jersey:
Dressiantha bicarpellata gen. et sp. nov. (Cappara-
les). American Journal of Botany, 85(7), 964–974.
147
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
Gentry, A. (1995). Diversity and floristic composition
of neotropical dry forests. In S. H. Bullock, H. A.
Mooney, & E. Medina (Eds.), Seasonally Dry Tro-
pical Forests (pp. 146–194). Cambridge University
Press.
Harmon, L. J., Weir, J., Brock, C., Glor, R. E., & Challen-
ger, W. (2008). GEIGER: Investigating evolutionary
radiations. Bioinformatics, 24, 129–131.
Herazo-Vitola, F., Mendoza-Cifuentes, H., & Mercado-
Gómez, J. (2017). Estructura y composición florística
del bosque seco tropical en los Montes de María
(Sucre – Colombia). Ciencia en Desarrollo, 8(1),
79–90.
Hernández, C. E., Rodríguez-Serrano, E., Avaria-Llautu-
reo, J., Inostroza-Michael, O., Morales-Pallero, B.,
Boric-Bargetto, D., Canales-Aguirre, C. B., Marquet,
P. A., & Meade, A. (2013). Using phylogenetic
information and the comparative method to evaluate
hypotheses in macroecology. Methods in Ecology and
Evolution, 4(5), 401–415.
Hernández-Hernández, T., Brown, J. W., Schlumpberger,
B. O., Eguiarte, L. E., & Magallón, S. (2014). Beyond
aridification: multiple explanations for the elevated
diversification of cacti in the New World Succulent
Biome. New Phytologist, 202(4), 1382–1397.
Hernández-Hernández, T., Colorado, W. B., & Sosa, V.
(2013). Molecular evidence for the origin and evolu-
tionary history of the rare American desert monotypic
family Setchellanthaceae. Organisms Diversity &
Evolution, 13(4), 485–496.
Hijmans, R., Cameron, S., Parra, J., Jones, P., & Jarvis,
A. (2005). Very high resolution interpolated climate
surfaces for global land areas. International Journal
of Climatology. 25, 1965–1978.
Holmgren, P., Holmgren, N., & Barnett, L. (1990). Index
Herbariorum. Part I: The Herbaria of the World.
Octava edición (Octava ed.). International Associa-
tion for Plant Taxonomy - The New York Botanical
Garden.
Ingram, T., & Mahler, D. L. (2013). SURFACE: detec-
ting convergent evolution from comparative data
by fitting Ornstein-Uhlenbeck models with stepwise
Akaike Information Criterion. Methods in Ecology
and Evolution, 4(5), 416–425.
Kers, L. E. (2003). Capparaceae. In K. Kubitzki, & C.
Bayer (Eds.), The families and genera of vascular
plants: V Flowering plants, dicotyledons: Malvales,
Capparales, and non-betalain Caryophyllales (pp.
36–56). Springer.
Lavin, M. (2006). Floristic and geographic stability of
discontinuous seasonally dry tropical forests explains
patterns of plant phylogeny and endemism. In R.
Pennington, J. Ratter, & G. Lewis (Eds.), Neotro-
pical savannas and seasonally dry forests: plant
biodiversity, biogeographic patterns and conserva-
tion (pp. 433–447). CRC Press.
Lewis, L., & Mccourt, R. M. (2004). Green algae and the
origin of land plants. American Journal of Botany,
91(10), 1535–1556.
Lorea-Hernández, F. G. (2004). Capparaceae. In J. Rze-
dowski Rotter, & G. Calderón de Rzedowski (Eds.),
Flora del Bajío y de regiones adyacentes. Insituto de
Ecologia A.C. y CONABIO.
Mercado-Gómez, J., & Escalante, T. (2018). Areas of
endemism of the Neotropical species of Capparaceae.
Biological Journal of the Linnean Society, 126(3),
507–520.
Mercado-Gómez, J., & Escalante, T. (2020). Track analysis
of Neotropical species of Capparaceae. Australian
Systematic Botany, 33, 129–136.
Mercado-Gómez, J., Gonzales, M., & Morales-Puentes, M.
E. (2019). Synopsis of Capparaceae to the flora of
Colombia. Rodriguésia, 70(e00232018), 1–23.
Mercado-Gómez, J., & Morales-Puentes, M. E. (2020). A
new species of Capparidastrum (Capparaceae Juss.)
from the Cauca inter Andean valley of Colombia.
Phytotaxa, 439(3), 276–286.
Mercado-Gómez, J., Prieto-Torres, D. A., Gonzalez, M.,
Morales-Puentes, M., Escalante, T., & Rojas, O.
(2020). Climatic affinities of neotropical species of
Capparaceae: an approach from ecological niche
modelling and numerical ecology. Botanical Journal
of The Linnean Society, 193, 1–13.
Michel, P., Payton, I. J., Lee, W. G., & During, H. J. (2013).
Impact of disturbance on above-ground water storage
capacity of bryophytes in New Zealand indigenous
tussock grassland ecosystems. New Zealand Journal
of Ecology, 37(1), 114–126.
Moore, W., & Robertson, J. A. (2014). Explosive adaptive
radiation and extreme phenotypic diversity within
ant-nest beetles. Current Biology, 24(20), 2435–2439.
Morrone, J. (2014). Biogeographical regionalisation of the
Neotropical region. Zootaxa, 3782(1), 1–110.
Münkemüller, T., Boucher, F. C., Thuiller, W., & Lavergne,
S. (2015). Phylogenetic niche conservatism – com-
mon pitfalls and ways forward. Functional Ecology,
29(5), 627–639.
Murphy, P. G., & Lugo, A. E. (1986). Ecology of tropical
dry forest. Annual Review of Ecology and Systema-
tics, 17, 67–88.
Newman, M. (2007). Capparaceae Juss. In R. Medina
Lemos (Ed.), Flora del valle de Tehuacán-Cuicatl-an.
Instituto de Biología, Universidad Nacional Autóno-
ma de México.
148 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 132-148, January-December 2022 (Published Mar. 02, 2022)
Olson, D., Dinerstein, E., Wikramanayake, E., Burgess,
N., Powell, G., Underwood, E., D’Amico, J., Itoua,
I., Strand, H., Morrison, J., Loucks, C., Allnutt, T.,
Ricketts, T., Kura, Y., Lamoreux, J., Wettengel, W.,
Hedao, P., & Kassem, K. (2001). Terrestrial eco-
regions of the world: a new map of life on Earth.
Bioscience, 51(11), 933–938.
Pagel, M. D. (2002). Modelling the evolution of conti-
nuously varying characters on phylogenetic trees.
In P. L. MacLeod, & N. Foley (Eds.), Morphology,
shape and phylogeny (pp. 269–286). Taylor and
Francis.
Paun, O., Turner, B., Trucchi, E., Munzinger, J., Chase,
M. W., & Samuel, R. (2016). Processes driving the
adaptive radiation of a tropical tree (Diospyros, Ebe-
naceae) in New Caledonia, a biodiversity hotspot.
Systematic Biology, 65(2), 212–227.
Pennington, R. T., Lavin, M., & Oliveira-Filho, A. (2009).
Woody plant diversity, evolution, and ecology in the
tropics: Perspectives from seasonally dry tropical
forests. Annual Review of Ecology, Evolution, and
Systematics, 40(1), 437–457.
Pennington, R. T., Lavin, M., Prado, D. E., Pendry, C. A.,
Pell, S. K., & Butterworth, C. A. (2004). Historical
climate change and speciation: neotropical seasonally
dry forest plants show patterns of both Tertiary and
Quaternary diversification. Philosophical Transac-
tions of the Royal Society of London Series B: Biolo-
gical Sciences, 359(1443), 515–538.
Prieto-Torres, D. A., & Rojas-Soto, O. R. (2016). Recons-
tructing the Mexican Tropical Dry Forests via an
autoecological niche approach: reconsidering the
ecosystem boundaries. PLoS ONE, 11(3), e0150932.
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., &
Suchard, M. A. (2018). Posterior Summarization in
Bayesian Phylogenetics Using Tracer 1.7. Systematic
Biology, 67(5), 901–904.
Revell, L. J. (2012). phytools: an R package for phylogene-
tic comparative biology (and other things). Methods
in Ecology and Evolution, 3(2), 217–223.
Ruiz-Zapata, T. (2005). Capparis L. (Capparoideae-Cappa-
raceae) en el estado Trujillo, Venezuela. Ernestia,
15(1-4), 27–50.
Ruiz-Zapata, T. (2006). Capparis L. subgénero Calanthea
DC. en Venezuela. Ernstia, 16(2), 113–127.
Särkinen, T., Pennington, R. T., Lavin, M., Simon, M.
F., & Hughes, C. E. (2012). Evolutionary islands
in the Andes: persistence and isolation explain high
endemism in Andean dry tropical forests. Journal of
Biogeography, 39(5), 884–900.
Sexton, J., Montiel, J., Shay, J., Stephens, M., & Slatyer,
R. (2017). Evolution of ecological niche breadth.
Annual Review of Ecology, Evolution, and Systema-
tics, 48(1), 183–206.
Soberon, J., & Peterson, T. (2005). Interpretation of models
of fundamental ecological niches and species’ distri-
butional areas. Biodiversity Informatics, 2, 1–10.
Stroud, J., & Losos, J. (2016). Ecological opportunity and
adaptive radiation. Annual Review of Ecology, Evolu-
tion, and Systematics, 47(1), 507–532.
Tan, J., Slattery, M. R., Yang, X., & Jiang, L. (2016). Phylo-
genetic context determines the role of competition in
adaptive radiation. Proceedings of the Royal Society
B: Biological Sciences. 283(1833), 20160241.
Thiers, B. (January 2018). Index Herbariorum: a global
directory of public herbaria and associated staff.
New York Botanical Garden. http://sweetgumnybg
org/ih
Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environ-
mental niche equivalency versus conservatism: quan-
titative approaches to niche evolution. Evolution,
62(11), 2868–2883.
Willis, C. G., Franzone, B. F., Xi, Z., & Davis, C. C.
(2014). The establishment of Central Americanm
igratory corridors and the biogeographic origins of
seasonally dry tropical forests in Mexico. Frontiers
in Genetics, 5(433), 1–14.
