Research
Insights into the historical construction of species-rich
Mesoamerican seasonally dry tropical forests: the diversification
of Bursera (Burseraceae, Sapindales)
J. Arturo De-Nova1, Rosalinda Medina1, Juan Carlos Montero1, Andrea Weeks2, Julieta A. Rosell1, Mark E. Olson1,
Luis E. Eguiarte3 and Susana Magallón1
1
Departamento de Botánica, Instituto de Biologı́a, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico; 2George Mason University, Fairfax, VA, USA; 3Departamento de
Ecologı́a Evolutiva, Instituto de Ecologı́a, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico
Summary
Author for correspondence:
Susana Magallón
Tel: +52 55 5622 9087
Email: s.magallon@ibiologia.unam.mx
Received: 15 June 2011
Accepted: 19 August 2011
New Phytologist (2011)
doi: 10.1111/j.1469-8137.2011.03909.x
Key words: aridification, Bursera,
dated phylogenies, diversification rate,
geographical structure, Mesoamerica, niche
conservatism, seasonally dry tropical forests.
• Mesoamerican arid biomes epitomize neotropical rich and complex biodiversity. To document some of the macroevolutionary processes underlying the vast species richness of Mesoamerican seasonally dry tropical forests (SDTFs), and to evaluate specific predictions about
the age, geographical structure and niche conservatism of SDTF-centered woody plant
lineages, the diversification of Bursera is reconstructed.
• Using a nearly complete Bursera species-level phylogeny from nuclear and plastid genomic
markers, we estimate divergence times, test for phylogenetic and temporal diversification
heterogeneity, test for geographical structure, and reconstruct habitat shifts.
• Bursera became differentiated in the earliest Eocene, but diversified during independent
early Miocene consecutive radiations that took place in SDTFs. The late Miocene average age
of Bursera species, the presence of phylogenetic geographical structure, and its strong conservatism to SDTFs conform to expectations derived from South American SDTF-centered
lineages.
• The diversification of Bursera suggests that Mesoamerican SDTF richness derives from high
speciation from the Miocene onwards uncoupled from habitat shifts, during a period of
enhanced aridity resulting mainly from global cooling and regional rain shadows.
Introduction
The Neotropical Realm is unparalleled in its biotic complexity
(Gentry, 1982a; Graham, 2010). The northern Neotropical
region geologically corresponds to southwestern Laurasia. It is
occupied today by Mexico and Central America, and is here
loosely referred to as ‘Mesoamerica’. It includes, but is not limited to, the Mesoamerican Biodiversity Hotspot (Myers et al.,
2000), and encompasses a vast diversity of habitats, functional
adaptations, and species richness. Substantial efforts to document
Mesoamerican biodiversity have been ongoing for centuries (e.g.,
Sessé & Mociño, 1887; Hernández, 1942; CONABIO, 2008).
However, its sheer richness, overlaid on an extensive and physically complex territory, have rendered these fundamental efforts
still incomplete. Very little is known about the main evolutionary
processes underlying high species richness in different Mesoamerican biomes. Is it caused by high speciation, or by low
extinction? Is it derived from temporally circumscribed speciation
bursts, or from long-term species accumulation? What is the
relative relevance of in situ diversification vs the prevalence of
immigrants? The main aim of this study is to investigate the
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evolutionary processes that contribute to high species richness in
a particular biome in Mesoamerica.
Arid biomes are prominent in Mesoamerica, providing
emblematic landscapes and a substantial part of its biodiversity.
While less diverse than wet forests, Mesoamerican arid biomes
are richer than their South American counterparts (Gentry,
1982a; Lott et al., 1987; Trejo & Dirzo, 2002; Villaseñor, 2004;
Pennington et al., 2009). Seasonally dry tropical forests (SDTFs)
encompass a variety of plant associations, from relatively moist
tall forests to dry, succulent-rich scrubs, that grow on fertile soils
where rainfall is below 1800 mm yr)1, and receive < 100 mm
for 5–6 months (Pennington et al., 2009). They are fire- and
frost-intolerant, and, in South America, are distributed in small
isolated patches separated by areas that are wetter, colder, extremely arid, or at very high elevation (Pennington et al., 2009).
Contrary to other biomes (e.g. lowland rainforests; Gentry,
1982a) and biological lineages (e.g. hylid frogs, Wiens et al.,
2006), the richest Neotropical SDTFs are distant from the Equator, leading some workers to discuss an ‘inverse latitudinal diversity gradient’ (Gentry, 1995; Trejo & Dirzo, 2002). Lott et al.
(1987) documented 83–105 spp. km)2 at 19N in Chamela,
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Mexico, close to the northern end of the distribution of this vegetation type, a substantially higher richness than in sampled
South American dry forest sites with equivalent precipitation,
and much higher than predicted by the postulated linear
relationship between mean annual precipitation and Neotropical
plant species richness (Gentry, 1982b; Lott et al., 1987;
Trejo & Dirzo, 2002). In particular, Mexican SDTFs have
high degrees of endemism and a pronounced species turnover
displayed by very low among-site floristic similarity (Trejo &
Dirzo, 2002).
After its emergence from the North American epicontinental
sea in the early Tertiary, the area corresponding to central and
northern Mexico was at least somewhat arid because of its latitudinal position in the descending arm of the Hadley global convection cell and the rain shadows cast by the western and eastern
Mexican mountain ranges (Sierra Madre Occidental and Sierra
Madre Oriental, respectively) which resulted from orogenic processes starting in the middle Cretaceous and mostly culminating
by the late Eocene (Graham, 2010). Between the Miocene and
Pliocene, aridity was further enhanced by a global cooling process
that resulted in polar ice sheets and local volcanism that enhanced
rain shadows (Graham, 2010, pp. 60–66). In response to
Miocene aridification, preadapted lineages that existed in North
America in the middle Eocene expanded southwards and,
together with newly evolved species, represented the onset of the
vegetation of the contemporary Sonoran and Chihuahuan
Deserts (Graham, 2010, pp. 62–63). Climatic and fossil evidence, as well as molecular clock ages of SDTF-centered lineages
(Lavin et al., 2003, 2004; Pennington et al., 2004; Pirie et al.,
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2009; Schrire et al., 2009), congruently indicate that Neotropical
SDTFs may have arisen in North America during the middle
Eocene (Pennington et al., 2009).
Considering the early Cenzoic origin, aridity and patchy distribution of South American SDTFs, Pennington et al. (2009)
postulated that these attributes have shaped the evolution of resident
woody plant lineages. Seasonal dryness represents a barrier to
potential colonists not adapted to some degree of aridity. Their
patchy distribution separated by areas that are difficult to surmount causes limited dispersal of propagules and pollen. These
barriers to migration, combined with their prolonged existence,
have resulted in a distinctive species composition for each patch.
As a consequence, South American SDTFs are compositionally
stable, dispersal-limited systems with high among-patch beta
diversity, which is positively correlated with geographical distance
(Linares-Palomino et al., 2011). SDTF-centered lineages consequently include ancient species and exhibit strong geographic
structure in their phylogenies (Pennington et al., 2009). Moreover, South American SDTF lineages exhibit strong niche conservatism where closely related species share the same type of
habitat, and habitat shifts are strongly directional: predominantly
from SDTFs to other types of vegetation (Pennington et al.,
2009). Mesoamerican SDTFs, while sharing with their South
American counterparts aridity and origin since at least the
Miocene, occupy a variety of physical conditions (e.g. edaphic,
altitudinal), a wide latitudinal range, and have a continuous distribution over extensive areas (e.g. the Mexican Pacific slope and
the Balsas river basin; Fig. 1), which is unusual for other
Neotropical SDTFs (Trejo & Dirzo, 2002).
Fig. 1 Main areas of Bursera distribution in seasonally dry tropical forests (SDTFs). The colored areas represent nine main disjunct areas of distribution of
Bursera in SDTFs, delimited mainly by considering species distributions (see main text). SDTFs are continuously distributed among several of these areas.
Nevertheless, the distribution of Bursera species is discontinuous as a result of altitudinal barriers. Map based on Brown et al. (2007).
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To document some of the diversification processes underlying
the high species richness of Mesoamerican SDTFs, and to evaluate if the old species age, high geographical structure and
directionality of habitat shifts observed for South American
SDTF-centered lineages prevail in their Mesoamerican counterparts, we use the genus Bursera (Burseraceae, Sapindales) as a
study system. Bursera is arguably the most distinctive physiognomic component of Mesoamerican SDTFs. It includes c. 107
species which, except for B. tonkinensis from northern Vietnam,
are approximately distributed between northern Mexico and
northern South America (Fig. 1). Bursera’s diversification has
been linked with the southward expansion of SDTFs in North
America in response to the uplift of the Sierra Madre Occidental
and the Mexican Transvolcanic Belt (Becerra, 2005; CevallosFerriz & González-Torres, 2005; Dick & Wright, 2005). The
strong association of Bursera with SDTFs has prompted attempts
to reconstruct the history of this vegetation type in Mexico on
the basis of the diversification of Bursera (Becerra, 2005; but see,
e.g. Dick & Wright, 2005).
Here we estimate phylogenetic relationships for a nearly complete representation of Bursera species based on one plastid and
four nuclear molecular markers. To document the diversification
process leading to Bursera species diversity, we estimate the
timing of lineage splitting and test for significant diversification
heterogeneity among phylogenetic branches and through time.
To evaluate specific predictions about SDTF-centered lineages
(Pennington et al., 2009), we obtain the average age of Bursera
species; conduct tests of geographical structure; and reconstruct
habitat shifts. We expect the following: a pre-Pliocene age for
most Bursera species, particularly for those centered in SDTFs;
the presence of geographical structure in its phylogeny; and
directional habitat shifts predominantly from SDTFs to other
vegetation types.
Materials and Methods
Research 3
Phylogenetic analyses
The sequences of each locus were aligned with MUSCLE (Edgar,
2004), and adjusted with Se-Al v.2.0a11 Carbon (Rambaut,
2002). The best fit model for each locus was identified with the
Akaike Information Criterion (AIC) implemented in ModelTest
v3.06 (Posada & Crandall, 1998), as follows: TVM+G for ETS;
GTR+I+G for ITS; K91uf+G for PEPC; HKY+G for NIAi3; and
HKY+G for psbA-trnH. Parsimony analyses were conducted
independently for each locus, using NONA (Goloboff, 1999)
spawned in WinClada (Nixon, 2002), and resulted in trees displaying weakly supported incongruences (results available from
the authors). Each of the five loci, and a concatenated five-loci
matrix, were analyzed with MrBayes v3.1.2 (Huelsenbeck &
Ronquist, 2001). Details of Bayesian phylogenetic analyses are
provided in Methods S1. The maximum a posteriori (MAP) tree
topology derived from the five-loci analysis was used as a working
hypothesis of phylogenetic relationships.
Divergence time estimation
Estimation of Bursera divergence times was done in two steps.
First, the age of crown group Burseraceae was estimated using
rbcL and atpB sequences for a representation of 28 order-level
eudicot clades, and including the crown group of Burseraceae
(Table S2). Ages were estimated with the uncorrelated lognormal
relaxed clock available in BEAST v1.4.8 (Drummond &
Rambaut, 2007), calibrated with the earliest fossil tricolpate
pollen grains plus 17 fossil-derived minimum-age constraints
(Table S3). In the second step, the mean age and credibility
interval of the Burseraceae crown node estimated previously were
assigned as root height priors to the Bursera data set, and used to
estimate divergence times among Bursera species. Dating was
conducted with the same method as described earlier, and
included five fossil-derived minimum age constraints (Table S4).
Dating analyses are described in detail in Methods S1.
Taxa and data
Ninety-three species of Bursera, from a total of c. 106, were
sampled from their natural distributions in the American continent. Species of Commiphora and representatives of the main
lineages within Burseraceae were also included. Species of Searsia
and Rhus (Anacardiaceae) were included as outgroups. Data
for phylogenetic analyses are the nucleotide sequences of
phosphoenolpyruvate carboxylase (fourth intron of the PEPC
gene), nuclear nitrate reductase (third intron of the NIAi3 gene),
internal and external transcribed spacers (ITS and ETS of the
nuclear ribosomal DNA, respectively), from the nuclear genome;
and the psbA-trnH intergenic spacer, from the plastid genome.
Previously published and newly generated sequences were combined (Supporting Information, Table S1). DNA extraction,
amplification and sequencing followed Rosell et al. (2010; details
provided in Methods S1). Sequence alignments are available
in TreeBase (http://purl.org/phylo/treebase/phylows/study/
TB2:S11329).
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Diversification rate analyses
The absolute rate of diversification (r) of Bursera, sections Bursera
and Bullockia, and several internal clades were calculated using a
maximum likelihood estimator that accounts for the possibility
of extinction (Magallón & Sanderson, 2001). Because absolute
rates of speciation (k) and extinction (l) are unknown, diversification rates were calculated under no extinction, and under a
high relative extinction rate (e = l ⁄ k = 0.0 and 0.9, respectively).
The presence of significant diversification rate changes was
evaluated among the branches of the phylogenetic tree, and
through time. Significant phylogenetic rate heterogeneity within
crown group Bursera was assessed with SymmeTREE v1.1 (Chan
& Moore, 2005), a method that, by calculating the combined
probability of the observed tree balance given constant stochastic
branching (equal rates Markov, ERM), identifies whether, and in
which branch, significant diversification increases have occurred
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(Chan & Moore, 2002). Because our phylogenetic analysis
included only 93 of the 106 known American Bursera species, 13
missing species were manually inserted into the MAP topology
on the basis of taxonomy and morphology (Table S5). The test
was based on one million ERM simulated trees, with polytomies
resolved through one million taxon size-sensitive random resolutions. Significant cumulative whole-tree probabilities of diversification rate change were identified through tail probability values
of the 0.025 and 0.975 frequentiles of the MP statistic (Chan &
Moore, 2002). Significant diversification rate shifts were located
through P-values associated to the D1 and D2 statistics for each
internal node, using 150 species for quick shift statistic calculation (Chan & Moore, 2005).
Significant temporal diversification rate heterogeneity was
tested with a maximum likelihood model-selection method
that fits time-constant and time-variable birth–death likelihood (BDL) models, which differ by being rate-constant or
rate-variable through time; allowing one or two temporal rate
changes; encompassing extinction; and considering that diversification is diversity-dependent, to a lineage through time
(LTT) plot (Rabosky, 2006a,b). Model selection is based on
the difference in AIC scores between the best-fitting rateconstant and rate-variable models (DAICRC). The LTT plot can
be used to identify the time(s) of diversification change. The
BDL method was implemented with LASER v2.3 (Rabosky,
2006b), using a LTT plot derived from the Bursera dated
phylogeny obtained with BEAST (Fig. 2). The test was conducted using yuleSim to determine the significance of the
observed DAICRC statistic by simulating 1000 trees with the
same number of taxa as in the input tree, and speciation rate
estimated under the pure-birth model.
Tests of geographical structure
Geographical structure among Bursera species was evaluated
through randomization tests and phylogenetic community structure analyses (Webb, 2000; Irwin, 2002; Lavin, 2006). We
identified nine main disjunct areas of distribution of Bursera in
SDTFs: (1) Baja California Peninsula; (2) NW Mexican Pacific
slope; (3) central Mexican Pacific coast; (4) Balsas river basin; (5)
Tehuacán Valley; (6) Gulf of Mexico; (7) Yucatán Peninsula; (8)
Central America-northern South America; and (9) the Caribbean
islands (Fig. 1). These areas were delimited by considering
observed Bursera species distributions, and modifying the SDTF
nuclei defined by Lott & Atkinson (2006), accounting for observations by Toledo Manzur (1982) and Dick & Wright (2005).
Whereas SDTFs are continuous over some of these areas, the
distribution of Bursera species is discontinuous because of their
inability to surmount high mountains that transverse these
regions. These nine geographical units were mapped onto the
Bursera MAP tree using parsimony optimization with MacClade
v4.07 (Maddison & Maddison, 2005). The observed number of
area transformations was then compared with the distribution of
the number of transformations of the same character states
mapped onto 1000 random trees generated with MacClade. If
observed area transformations involved substantially fewer steps
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than those on random trees, a strong geographic phylogenetic
structure was inferred.
The phylogenetic structure of each area was quantified using
PHYLOCOM (Webb, 2000; Webb et al., 2002, 2008). The net
relatedness index (NRI) and the nearest taxa index (NTI) were
estimated from Bursera phylogenetic relationships as depicted in
the MAP tree. High, low, and negative NRI and NTI values indicate that sister species have a high probability of occupying the
same (aggregated distribution), random, or different areas (overdispersed distribution), respectively. Significance of NRI and
NTI values were determined through a frequency distribution
of these values calculated for 10 000 randomly assigned geographical areas on the phylogeny.
Direction of habitat shifts
Field observations and species distribution data obtained from
published taxonomic accounts were used to determine the main
vegetation type preference of each sampled species of Bursera. We
then transformed all the listed vegetation types into four main
categories: seasonally dry tropical forests, tropical rainforests,
xerophytic scrubs, and oak forests. The ancestral vegetation type
of Bursera, and the direction of shifts, were reconstructed using
the maximum likelihood approach available in Mesquite v2.74
(Maddison & Maddison, 2010), which incorporates branch
length information into ancestral state inference. Reconstructions
assumed all transformations to be equiprobable (Mk1 model).
The procedure ‘trace over trees’ was used to summarize reconstructions over a set of 1000 chronograms chosen randomly from
among those sampled by BEAST (after the burn-in), including
only Bursera species. Trees were rooted with Commiphora, for
which a seasonally dry tropical forest was specified as its preferred
vegetation type.
Results
Phylogeny estimation
The aligned combined dataset for the five loci contained 109
taxa, including 93 Bursera species (Table S1). Bayesian Monte
Carlo Markov chains (MCMC) for the five combined loci
reached stationarity at c. 400 000 generations. The effective
sample size (ESS) of almost all estimated parameters is well above
200. The ‘compare’ plot produced by AWTY (Wilgenbusch
et al., 2004; available from the authors) suggests that parallel
MCMC runs achieved topological convergence. Thirty-one phylograms topologically identical to the MAP topology were found,
and one, including PP values, is shown in Fig. S1. Bayesian analysis recognized Bursera (posterior probability (PP) = 1.0) and
Commiphora (PP = 1.0) as monophyletic, forming a sister pair
(PP = 1.0). The deepest split within Bursera separates sections
Bursera and Bullockia (PP = 1.0 each). The deepest split within
section Bursera separates the Simaruba group (PP = 1.0) – the
‘mulatos’, including a nested Caribbean clade (PP = 1.0), from
the ‘cuajiotes’ (Burseras with exfoliating bark; PP = 1.0) consisting of the sister Fagaroides and Microphylla groups (PP = 0.97
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B. bolivarii
B. chemapodicta
B. medranoa
8.37
B. schlechtendalii
B. aptera
6.32
11.62
B. fagaroides
B. ariensis
8.47
13.75
B. trifoliata
B. discolor
6.79
B. staphyleoides
15.7
B. odorata
Fagaroides
5.11
B. vazquezyanesii
8.62
19.89
13.59
B. palaciosii
B. paradoxa
B. denticulata
B. morelensis
5.3
21.98
B. suntui
7.72
11.17
B. arida
B. galeottiana
14.21
B. microphylla
7.72
17.54
B. multifolia
23.31
B. rzedowskii
B. lancifolia
8.48
B. trimera
11.43
27.13
B. kerberii
16.3
B. confusa
Microphylla
10.95
30.32
B. multijuga
B. fragilis
B. crenata
1.81 B. nashii
B. sp. nov.
3.15
C. angustata
4.82
B. frenningae
1.45
8.27
Caribbean 11.72
B. inaguensis
B. shaferi
B. spinescens
14.42
B. grandifolia
5.45
B. instabilis
8.59
15.5
B. longipes
B. permollis
B. arborea
17.16
2.7
B. ovalifolia
3.86
B. krusei
6.77
Simaruba
B. cinerea
4.69
10.25
19.68
B. laurihuertae
B. attenuata
B. itzae
8.42
B. simaruba
16.65
B. standleyana
B. copallifera
4.63
B. excelsa
6
B. aspleniifolia
7.27
B. isthmica
8.65
B. sarukhanii
4.18
B. velutina
5.63
B. bicolor
7.65
9.58
B. hintonii
B. submoniliformis
4.1
B. vejarvazquezii
7.05
10.99
B. bippinata
B. cerasifolia
4.59
B. hindsiana
8.85
Copallifera
B. stenophylla
7.52
11.72
B. palmeri
B. laxiflora
7.08
B. filicifolia
9.21
B. ribana
2.82
10.14
B. glabra
B. mcvaughiana
2.76 B. madrigalii
B. xochipalensis
6.63
13.69
B. glabrifolia
9.8
B. epinnata
5.18
B. tomentosa
10.25
B. infiernidialis
6.55
B. penicillata
11.25
B. linanoe
3.68
B. simplex
15.1
7.71
B. coyucensis
12.63 9.31
B. citronella
Glabrifolia
B. fragrantissima
6.35
B. heteresthes
10.86
B. graveolens
6.08
16.91
B. steyermarkii
B. bonetti
8.26
B. mirandae
11.82
B. esparzae
B. pontiveteris
19.83
6.87
B. altijuga
13.69
B. biflora
10.15
B. cuneata
B. sarcopoda
B. tecomaca
C. africana
12.21
C. wrightii
14.98
C. campestris
19.24
C. leptophloeos
21.54
24.51
C. edulis
27.6
C. grandifolia
C. neglecta
32.87
C. guillaumini
16.31
C. monstruosa
Canarium pilosum
2 30.71
Santiria griffithii
Boswellia sacra
Protium copal
Beiselia mexicana
5.55
7.73
4.33
Sect. Bursera
5
40.1
Bursera
49.43
3
54.75
4
60.72
1
43.46
Sect. Bullockia
63.86
Commiphora
64.92
c
Burseraceae
42.36
P al e o c e n e
Eocene
Oligocene
Miocen e
P aleog ene
60
50
40
Ne o g e n e
30
20
10
Pliocene
Q
Ma
Fig. 2 Timing of Bursera diversification. Chronogram derived from the maximum clade credibility tree estimated with the uncorrelated lognormal method
in BEAST. Mean ages and their 95% highest posterior density (HPD) are shown next to nodes. The red node (C) represents the calibration node. Green
numbered nodes were constrained with fossil-derived minimal ages as shown in Supporting Information, Table S4. Branches marked in red and orange
were identified by SymmeTREE as having significant and marginally significant increases in diversification, respectively.
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and 1.0, respectively), and the members of the Fragilis group,
forming an early diverging grade (Fig. S1).
Independent Bayesian analyses of the five loci (results available
from the authors) found low resolution at deep levels in the
phylogeny, but the sections inside Bursera, and the genus Commiphora, were always monophyletic. Whereas the trees obtained
with ITS, NIAi3, and psbA-trnH resolved Bursera as the monophyletic sister of Commiphora, trees obtained with ETS and
PEPC found Bursera to be paraphyletic, with section Bursera,
and section Bullockia, respectively, more closely related to
Commiphora. These relationships are weakly supported.
Divergence time estimation
The uncorrelated lognormal dating analyses in BEAST provided
an ESS of > 300 for the age of crown Burseraceae, and estimated
a mean age of 57.43 million yr (Myr) (63.35–51.77, 95% highest posterior density (HPD); results available from authors). This
estimate falls within the stratigraphic interval containing the
oldest fossil remains of Burseraceae (Bursericarpum aldwickense,
Ypresian, Eocene; Collinson, 1983; Table S4).
The combined MCMCs of the uncorrelated lognormal dating
analyses for Burseraceae provided ESS > 200 for age parameters.
The mean age for crown Burseraceae is 64.92 Myr (60.33–
69.67; Fig. 2). Ages of clades within Bursera, and their associated
errors, are available in Table 1 and Fig. 2. The average stem
group age of Bursera species is 7.92 Myr (SD = 6.10). The average age of Bursera species that typically inhabit SDTFs is
7.49 Myr (SD = 5.31); of species from xerophytic scrubs is
6.54 Myr (SD = 2.40); and from tropical rainforests is
11.16 Myr (SD = 4.75). Species from oak forests are older, being
on average 13.37 Myr (SD = 13.44). This average age is strongly
influenced by the early split of B. tecomaca, 43.46 Myr ago. The
average age of oak forest Bursera species, excluding B. tecomaca,
is 8.35 Myr (SD = 2.37).
Diversification rate analyses
Absolute diversification rates of Bursera were estimated as
0.0484 net speciation events per million yr (sp Myr)1) under a
high relative extinction rate (e = 0.9), and 0.0803 sp Myr)1
under no extinction (e = 0.0). Diversification rates estimated for
clades within Bursera are shown in Table 1. The MP statistic in
SymmeTREE detected significant diversification rate heterogeneity in the tree with tail probabilities of 0.0040 and 0.0289 for the
0.025 and 0.975 frequentiles, respectively. The D1 statistic
detected two branches where significant rate increases occurred
(Fig. 2): the branch subtending the most recent common ancestor (MRCA) of B. cuneata and B. copallifera (P = 0.0364), corresponding to section Bullockia, excluding B. tecomaca and
B. sarcopoda, and here referred to as the ‘nearly Bullockia clade’;
and the branch subtending the MRCA of B. multijuga and
B. bolivarii (P = 0.0430), corresponding to the ‘cuajiotes’,
excluding B. crenata and B. fragilis, and here referred to as the
‘nearly cuajiotes clade’. The D2 statistic detected a significant rate
change in the former branch (P = 0.0476), but a marginally
significant one in the latter (P = 0.0516). Marginally significant
rate changes were also detected in the branches subtending the
Table 1 Ages and diversification rates estimated for Bursera, including clades identified as resulting from significant (**) or marginally significant (*)
diversification rate increase, as detected by SymmeTREE
Clade
Burseraceae
Bursera – Commiphora split
Bursera
Section Bursera
Microphylla clade
Fagaroides clade
Simaruba clade
Caribbean clade
Nearly cuajiotes clade** (MRCA B.
multijuga – B. bolivarii)
Nearly Fagaroides clade* (MRCA
B. paradoxa – B. bolivarii)
Approximately Carribean clade*
(MRCA B. longipes – B. nashii)
Section Bullockia
Section Bullockia after B. tecomaca
Glabrifolia clade
Copallifera clade
Nearly Bullockia clade** (MRCA B.
cuneata – B. copallifera)
Glabrifolia plus Copallifera clades*
(MRCA B. steyermarkii – B. copallifera)
Crown group mean
age (95% HPD)
Stratigraphic interval
Age estimated by Number of
Becerra (2005)
species
r (e = 0.0) r (e = 0.9)
64.92 (60.33–69.67)
54.75 (50.61–58.96)
49.43 (45.38–53.77)
40.1 (35.31–45.33)
17.54 (12.17–23.41)
19.89 (14.62–25.88)
19.68 (13.15–26.84)
11.72 (7.36–16.51)
23.31 (17.30–29.45)
Early Paleocene (Danian)
Early Eocene (Ypresian)
Early Eocene (Ypresian)
Middle Eocene (Bartonian)
Early Miocene (Burdigalian)
Early Miocene (Burdigalian)
Early Miocene (Burdigalian)
Middle Miocene (Serravallian)
Latest Oligocene (Chattian)
NA
> 100
> 70
c. 50
c. 35
< 20
c. 30
NA
NA
–
–
106
59
9
16
26
11
31
–
–
0.0803
0.0844
0.0858
0.1045
0.1303
0.1455
0.1176
–
–
0.0484
0.0465
0.0304
0.0434
0.061
0.0546
0.0572
15.70 (11.23–20.78) Middle Miocene (Langhian)
NA
15
0.1283
0.0524
14.42 (9.64–19.94)
Middle Miocene (Langhian)
NA
14
0.1349
0.0541
43.46 (40.74–46.61)
19.83 (12.77–27.77)
12.63 (8.85–16.76)
11.72 (8.36–15.79)
16.91 (11.30–22.55)
Middle Eocene (Lutetian)
Early Miocene (Burdigalian)
Middle Miocene (Serravallian)
Middle Miocene (Serravallian)
Early Miocene (Burdigalian)
c. 40
> 20
< 20
c. 20
NA
47
–
16
21
45
0.0726
–
0.1646
0.2006
0.1841
0.0384
–
0.0684
0.0893
0.0967
13.69 (9.65–17.95)
Middle Miocene (Langhian)
NA
36
0.2111
0.1061
HPD, highest posterior density; MRCA, most recent common ancestor; NA, not applicable.
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MRCA of B. paradoxa and B. bolivarii, corresponding to the
Fagaroides clade excluding B. denticulata, and here referred to as
the ‘nearly Fagaroides clade’ (PD1 = 0.0762 and PD2 = 0.0952);
the MRCA of B. steyermarkii and B. colpallifera, corresponding
to the Glabrifolia plus Copallifera clade (PD1 = 0.0835, PD2 =
0.0975); and the MRCA of B. longipes and B. nashii, corresponding to the Caribbean clade plus B. longipes, B. instabilis
and B. grandifolia, and here referred to as the ‘approximately
Caribbean clade’ (PD1 = 0.0989; Fig. 2). The absolute diversification rates associated with these rate increases are shown in
Table 1.
The BDL analysis rejected the null hypothesis of temporally
homogeneous diversification rates within Bursera (DAICRC =
33.0863; P < 0.001, Table S6). The yule3rate model, which
includes two diversification rate shifts and no extinction, was
found to fit the data best (AIC = )50.6052). The (log) number
of lineages and the rate shifts under the best rate-variable model
were plotted as a function of time (Fig. 3). According to the scenario suggested by the yule3rate model, Bursera started to diversify with a rate r1 = 0.0481 sp Myr)1. A shift in diversification
rate occurred at ts1 = 19.89 Myr, increasing to r2 = 0.1312 sp
Myr)1, followed by a shift at ts2 = 4.10 Myr, decreasing to
r3 = 0.0214 sp Myr)1.
Randomization tests with MacClade detected significant geographical structure in phylogenies (P < 0.01, Fig. 4). The nine
main distribution areas of Bursera in STDFs were optimized with
a minimum of 88 transformations on the MAP tree, while optimization on each of 1000 random trees yielded a range of 96–
108 steps, indicating that sister species in Bursera have a high
likelihood of being confined to the same geographical region.
The phylogenetic community structure analysis in PHYLOCOM
(Table 2) showed that most of the geographic structure is condensed in four STDF units: Caribbean islands, Balsas river basin,
Baja California Peninsula, and Tehuacán Valley, with significant
5.0
31
0214
r 3 = 0.
4.5
4.0
30
r2
=
3.5
3.0
29
2.5
r1 =
481
0.0
28
st1 = 19.88
1.0
Log-L of rate shifts
0.
13
12
Loge (number of lineages)
st2 = 4.1
1.5
27
0.5
0
60
50
40
30
20
10
0
26
Time before present (Myr)
Fig. 3 Diversification analysis of Bursera. The red line indicates the lineage
through time (LTT) plot derived from nodal divergence times obtained
from uncorrelated lognormal dating in BEAST. The black line indicates likelihood of changes of diversification rate through time under the best-fit
diversification model.
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200
190
180
170
160
150
140
130
120
110
100
90
80
70
60
50
40
30
20
10
0
*
88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108
Number of steps
Fig. 4 Test of geographical structure. Histogram showing the number of
shifts for seasonally dry tropical forest (STDF) optimized via parsimony on
1000 random equiprobable phylogenetic trees of Bursera. The analysis
optimized nine geographical areas (see main text) with a minimum of 88
transformations on the maximum a posteriori tree. Optimizations on each
of 1000 random trees yielded a range of 96–108 steps. The observed
reconstruction falls outside this distribution (asterisk), and is considered
indicative of substantial geographical structure.
positive NTI values (P < 0.05), indicating that shared area of
occupancy predicts phylogenetic relatedness.
Tests of geographical structure
2.0
Number of trees
Research 7
Direction of habitat shifts
The vegetation type that each Bursera species most commonly
occupies is shown in Fig. 5. Of the 93 sampled species of Bursera,
70 (75.27%) typically inhabit SDTFs; 13 (13.98%) occupy xerophytic scrubs; seven (7.53%) inhabit oak forests; and three
(3.22%) occupy tropical rainforests. A SDTF was reconstructed
as the ancestral vegetation type of Bursera (LH: 0.9478) and of its
two sections (section Bursera: LH = 0.9769; section Bullockia:
LH = 0.9181). A SDTF was reconstructed as the most likely
state for most internal nodes (Fig. 5). Shifts to other vegetation
types always involved a change from SDTF to a different vegetation type, except for one possible reversion. There were nine
shifts to xerophytic scrubs: one in the Glabrifolia clade (occurring
after 5.18 Myr); three in the Copallifera clade (the first after 7.08
Myr, the second after 4.59 Myr, and the third after 2.82 Myr);
two in section Bullockia outside the Glabrifolia and Copallifera
clades (one after 10.15 Myr, and another after 6.87 Myr); two in
the Fagaroides clade (one after 5.11 Myr, and another after
4.33 Myr); and one in the Microphylla clade (between 17.54
and 14.21 Myr) with an apparent reversion to SDTF (between
7.72 and 5.3 Myr). There were seven shifts to oak forests: two in
the Copallifera clade (one after 7.52 Myr, and another after
7.05 Myr); three in section Bullockia outside the Glabrifolia and
Copallifera clades (the first after 43.46 Myr, the second after
11.82 Myr, and the last after 10.15 Myr); and two in the Fagaroides clade (one after 8.47 Myr and the other after 5.11 Myr). A
single shift to tropical rainforest was reconstructed, occurring
within the Simaruba clade (between 19.68 and 16.65 Myr;
Fig. 4).
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Table 2 Net relatedness and nearest taxa indices estimated with PHYLOCOM using the independent swap algorithm for 1000 runs
Area
Accesions (n)
NRIa
Quantileb
NTIc
Quantileb
Baja California Peninsula*
NW Mexican
Pacific slope
Central Pacific coast
Balsas river basin*
Tehuacan Valley*
Gulf of Mexico
Yucatán Peninsula
Central America-northern South America
Caribbean islands*
7
18
0.7294
0.3494
799
641
1.9384
0.0176
980
512
34
44
19
7
4
11
8
0.0672
0.4428
0.2253
1.0017
1.4247
1.2945
7.2856
547
681
598
844
912
900
1000
0.8613
3.2771
1.7152
1.0895
1.5073
0.6533
3.9990
817
1000
959
868
941
759
1000
SDTF: 0.9478
SDTF: 0.9962
XS: 0.6863
Tropical rain forest
Seasonally dry tropical forest
Oak forest
Xerophytic scrub
SDTF: 0.8949
TRF: 0.9830
33.9
Eocene
Paleogene
23.03
Oligocene
Glabrifolia
Caribbean
Simaruba
Sect. Bursera
SDTF: 0.9769
Fagaroides
Bursera
Microphylla
XS: 0.9655
Sect. Bullockia
SDTF: 0.9181
B. tecomaca
B. pontiveteris
B. altijuga
B. biflora
B. cuneata
B. bonetti
B. mirandae
B. esparzae
B. aspleniifolia
B. copallifera
B. excelsa
B. isthmica
B. hintonii
B. bicolor
B. sarukhanii
B. velutina
B. bippinnata
B. submoniliformis
B. vejarvazquezii
B. cerasifolia
B. hindsiana
B. stenophylla
B. palmeri
B. laxiflora
B. filicifolia
B. ribana
B. glabra
B. mcvaughiana
B. citronella
B. coyucensis
B. linanoe
B. simplex
B. epinnata
B. tomentosa
B. glabrifolia
B. madrigalii
B. xochipalensis
B. infernidialis
B. penicillata
B. fragrantissima
B. heteresthes
B. graveolens
B. steyermarkii
B. sarcopoda
B. aptera
B. fagaroides
B. bolivarii
B. chemapodicta
B. medranoa
B. schlechtendalii
B. ariensis
B. trifoliolata
B. discolor
B. staphyleoides
B. odorata
B. vazquezyanesii
B. palaciosii
B. paradoxa
B. denticulata
B. arida
B. morelensis
B. suntui
B. galeottiana
B. microphylla
B. multifolia
B. rzedowskii
B. confusa
B. multijuga
B. kerberi
B. lancifolia
B. trimera
B. fragilis
B. crenata
B. arborea
B. ovalifolia
B. krusei
B. cinerea
B. laurihuertae
B. attenuata
B. grandifolia
B. instabilis
B. longipes
B. frenningae
B. inaguensis
B. nashii
B. sp. nov.
C. angustata
B. shaferi
B. spinescens
B. permollis
B. standleyana
B. itzae
B. simaruba
Commiphora
Copallifera
NRI, net relatedness index; NTI, nearest taxa index.
a
Quantifies the degree of aggregation in the phylogeny of the sampled areas. Higher values indicate phylogenetic structure.
b
The number of random trees in which NRI and NTI measures were lower than the actual estimate (‡ 950 is significant*).
c
Quantifies the degree to which the sister group of any given taxon inhabits the same area. Higher values indicate phylogenetic structure.
5.33
Miocene
Neogene
1.81
Plio
Q
Fig. 5 Reconstruction of habitat shifts. The Mk1 model reconstructed seasonally dry tropical forest (SDTF) as the ancestral habitat for Bursera, and for most
of the internal nodes in the phylogeny. Shifts to xerophytic scrubs (XS) and to oak forest occurred independently in nearly all clades within Bursera, whereas
shifts to tropical rain forest (TRF) occurred only in the Simaruba clade.
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Discussion
Time and mode of diversification in Bursera
Our phylogenetic results are based on a nearly complete specieslevel representation of Bursera, a sample of major lineages
within Burseraceae, and the combined sequences of one plastid
and four nuclear markers. The Vietnamese B. tonkinensis is
apparently more closely related to Commiphora than to Bursera
(Weeks & Simpson, 2007); hence, its absence in these analyses
is unlikely to compromise the phylogenetic, dating and diversification results.
The origin of family Burseraceae, represented by the divergence of Beiselia mexicana from the remainder of the family, is
here estimated in the earliest Paleocene (Danian; 64.92 Myr).
This age is slightly older than the one estimated by Weeks et al.
(2005; 60 ± 1.9 Myr), and both fall within the same stratigraphic interval. The divergence of Bursera and Commiphora
occurred in the earliest Eocene (Ypresian; very close to the age
estimated by Weeks & Simpson, 2007), soon followed by the
split between sections Bursera and Bullockia (Fig. 2). Most of the
ages here obtained are much younger than previous estimates
(Becerra, 2003, 2005), including the split between Commiphora
and Bursera (c. 45 Myr younger) and the divergence of sections
Bursera and Bullockia (c. 20 Myr younger; Table 1). These age
differences, most likely the result of different calibration strategies, suggest the need for a reconsideration of the postulated
> 100 Myr association between the sister pairs DiamphidiaBlepharida herbivores and their Commiphora-Bursera hosts
(Becerra, 2003).
Whereas the genus Bursera is c. 50 Myr old, most of its extant
species are much younger – namely, the Microphylla, Fagaroides
and Simaruba clades, within section Bursera, and section Bullockia after the divergence of B. tecomaca, all started to generate
extant species between 20 and 17.5 Myr ago, a time when the
Miocene aridification trend reached its peak (Graham, 2010).
Sections Bursera and Bullockia exhibit parallel waiting times
between their differentiation in the earliest Eocene and the onset
of their radiation in the Miocene (Fig. 2). The crown groups of
both sections were here constrained to have fairly old minimal
ages. If these minimal ages are incorrect, the long temporal separation between each clade’s differentiation and radiation, and
their inferred diversification modes might be artifactual. We
nevertheless believe that the long temporal separation between
the origin and the diversifications of sections Bursera and Bullockia
are real, because (1) two independent evaluations (Weeks et al.,
2005 and this study) found similarities between the early-middle
Eocene B. inaequalateralis, and the early Oligocene B. serrulata,
and members of sections Bullockia and Bursera, respectively; (2)
other fossils confidently assigned to Burseraceae are older than
the two previous fossils; (3) ages estimated for the crown nodes of
sections Bursera and Bullockia (40.1 and 43.46 Myr, respectively)
are older than their minimal age constraints (33.9 and 40.4 Myr,
respectively); and (4) the crown groups of each of the two
sections and their respective diversifications are each separated by
a long phylogram branch (Fig. S1).
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The absolute diversification rate estimated for Bursera is similar
to that of angiosperms as a whole (r = 0.089, given e = 0.0;
Magallón & Sanderson, 2001), and lower than that of Sapindales
(r = 0.1114 with e = 0.0, and r = 0.0879 with e = 0.9; Magallón
& Castillo, 2009). However, several of its subclades have very
high rates (e.g. r = 0.2006 and 0.2111 in the Copallifera and
Glabrifolia plus Copallifera clades, respectively; Table 1). Two
significant rate increases led to the diversification of the nearly
Bullockia clade and the nearly cuajiotes clade c. 17 and 23 Myr
ago (Fig. 2), which together generated over 70% of Bursera’s
extant species. Absolute diversification rates associated with these
clades include some of the highest within the genus (Table 1).
The independent radiations within Bursera are unlinked from
habitat shifts, as indicated by the fact that most of the reconstructed habitat shifts took place long after the most likely time
when an increase in diversification occurred; that the branches
where habitat shifts were reconstructed were not detected as
having increased diversification rates (Fig. 5); and that the starting and ending nodes of all branches where increased rates were
detected (see earlier; Figs 2, 5) were reconstructed as a SDTF.
The test for temporal diversification rate heterogeneity identified a model with no extinction and two rate shifts as best fitting
the LTT Bursera plot (Fig. 3). The first rate change was an
increase at 19.89 Myr, during the early Miocene. The second rate
change was a decrease 4.01 Myr ago, during the early Pliocene.
This rate decrease, which appears as a flattening of the LTT plot
as it approaches the present (Fig. 3), might nevertheless be an
artifact of the 13 species that were not included in this analysis,
especially considering that some of them have been taxonomically
associated with species younger than 5 Myr. Clearly, high speciation played the major role in Bursera’s diversification. However,
the existence of Tertiary fossil representatives of sections Bursera
and Bullockia, outside Bursera’s present-day natural distribution,
suggests that extinction also had a role, albeit possibly a minor
one, in Bursera’s evolution. Furthermore, we wonder if a rate-variable diversification model that includes extinction can be confidently rejected in favor of a pure birth one, because according to
BDL model selection, the AIC score of the latter is only slightly
smaller than that of the former ()50.61 and )49.98, respectively;
see Quental & Marshall, 2009).
The combined results of dating analyses, diversification tests
and ancestral habitat reconstruction indicate that several independent lineages within Bursera began their diversification consecutively, and without involving habitat shifts, into extant diversity
during the first half of the Miocene, in a process characterized by
increased speciation. This reconstructed evolutionary history is
congruent with the postulated expansion of SDTFs as a consequence of enhanced aridity in northern and central Mexico
during the Miocene, mainly derived from global cooling and the
rain shadow cast by the final uplift of the Sierra Madre Occidental in the Eocene (Graham & Dilcher, 1995; Dick & Wright,
2005; Graham, 2010). Nevertheless, we think that there are no
simple links among Mesoamerican aridification, the expansion of
SDTFs, and Bursera diversification. Mesoamerican aridification
seems the consequence of complex interactions among global
tectonics that resulted in cooling and drying starting in the
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middle Eocene; regional orogeny that caused the uplift of the
Sierra Madre Occidental and Sierra Madre Oriental, and their
rain shadows, mainly between the late Cretaceous and the late
Eocene; and local post-Eocene volcanism and block faulting,
including the uplift of the Mexican Transvolcanic Belt in the
Miocene, which altered local drainage systems and enhanced rain
shadows (Graham, 2010, pp. 60–66). Given these complex and
prolonged interactions, it seems difficult to postulate a single causal event, let alone a narrow time interval, when Mesoamerican
aridity set in, triggering the expansion of SDTFs. Furthermore,
we lack elements to evaluate if the expansion of SDTFs in Mesoamerica and the diversification of Bursera occurred synchronously. It is possible that the expansion of this vegetation type (or
its Tertiary equivalent) predated the diversification of any of the
plant lineages that currently inhabit it. Our expectation regarding
the pre-Pliocene age of most Bursera species is based on the simple assumption that, by the onset of the Pliocene, arid conditions
were fully established in Mesoamerica.
including recent discoveries (e.g. Rzedowski & Calderón de
Rzedowski, 2008; León de la Luz & Pérez-Navarro, 2010) and
numerous endemics.
The observation that most Bursera species typically inhabit
SDTFs, together with the reconstruction of SDTF as the ancestral vegetation type for the genus and for most internal tree
nodes, documents a high degree of phylogenetic niche conservatism. Habitat shifts are relatively infrequent, and, except for a
reversion, all occurred from SDTFs to other vegetation types.
The largest number of shifts were into xerophytic scrubs – a
harsher, drier environment than SDTFs, and occurred independently in all major lineages within Bursera, except for the Simaruba clade. The number and distribution of shifts in the
phylogeny suggest that, whereas the possibility to occupy drier
environments may be a generalized preadaptation across Bursera
resulting from a plesiomorphic tolerance of aridity, the preadaptations to occupy substantially wetter environments may be
phylogenetically restricted.
Predictions for seasonally dry tropical forest-centered
lineages
Conclusions
Based on the premise that the physical attributes and patchy
distribution of South American SDTFs shape the evolutionary
history of resident woody plant lineages, Pennington et al.
(2009) predict the old age of their species; a high geographic
structure in their phylogenies; and niche conservatism with habitat shifts predominantly from SDTFs to other vegetation types.
The results here obtained for Bursera indicate that these predictions hold for Mesoamerican SDTFs. A substantial proportion of
Bursera species are endemic to, or preferentially inhabit, SDTFs.
All but four sampled Bursera species predate the Pleistocene, and
the average age of Bursera species centered in SDTFs is 7.49 Myr
(late Miocene).
The prediction that sister pairs of SDTF-centered woody plant
lineages will occupy the same SDTF nucleus (Pennington et al.,
2009) was supported by randomization tests and analyses of
phylogenetic community structure for Bursera. The geographic
structure of Bursera suggests a limited historical dispersal among
Mesoamerican SDTFs. However, it is somewhat weak in comparison with, for example, the South American robinioid legumes
Coursetia and Poissonia (Schrire et al., 2009). One possible interpretation is that the environmental and physical attributes of
South American SDTFs are less pronounced in Mesoamerica.
Specifically, Mesoamerican SDTFs usually occupy extensive continuous areas, and the barriers among disjunct nuclei are usually
less pronounced as those separating South American SDTF
patches. These differences would allow greater dispersal among
Mesoamerican SDTF nuclei and, hence, cause weaker phylogenetic geographical structure.
Some of the highest levels of Bursera phylogenetic community structure were detected in the Balsas river basin and the
Tehuacán Valley, both in central western Mexico, and in the
Baja California Peninsula and the Caribbean islands. These four
SDTF nuclei are present-day hotspots of Bursera diversification,
as exemplified by the high number of species they house,
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The reconstructed evolutionary history of Bursera provides
insights of the processes that led to high species richness in Mesoamerican SDTFs. Bursera differentiated in the earliest Eocene,
and soon after, split into its two main lineages. In the early
Miocene, these two lineages initiated in parallel and without
involving habitat change the diversifications that gave rise to most
of their extant species. These diversifications took place in a
context of enhanced aridity in north and central Mexico, resulting
from complex and temporally extended interactions among global
tectonics, regional orogenic activity, and local volcanism (Graham
& Dilcher, 1995; Dick & Wright, 2005; Graham, 2010). The
main process driving Bursera’s diversification was high speciation.
The late Miocene average age of Bursera species, the presence of
geographic structure in its phylogeny, and unequivocal niche conservatism conform to predictions derived from attributes of South
American SDTFs (Pennington et al., 2009).
The reconstructed evolutionary history of Bursera indicates
that at least some of the high species richness of Mesoamerican
SDTFs derives from increased within-habitat speciation rates,
from the early Miocene onwards, in the context of enhanced aridity. This scenario agrees with previous suggestions that lineages
mostly restricted to dry environments in Mexico resulted from
long periods of isolated evolution rather than rapid species generation (Rzedowski, 1962).
Acknowledgements
We thank R.T. Pennington and C. Hughes for critical discussions; P. Fine, M. Lavin and an anonymous reviewer for useful
observations; J.E. Morales Can, M.E. Véliz Pérez, R. Ramı́rez
Delgadillo and J. Pérez de la Rosa for field work help; J. Pérez
Camacho and C. Martı́nez Habibe for species samples; V. Patiño
for help with ancestral reconstructions; P. Maeda for contributing
Fig. 1; S.R.S. Cevallos Ferriz and L. Calvillo Canadell for geological information; and R. Tapia and G. Ortega Leite for technical
2011 The Authors
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help. The Coordinación de la Investigación Cientı́fica, Universidad Nacional Autónoma de México, provided postdoctoral funding to J.A.D.N. This research was partially funded by grants NSFDEB 0919179 to A.W.; CONACyT 2004-C01-46475 to L.E.E.
and M.E.O.; and PAPIIT-UNAM 202310 to S.M.
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Supporting Information
Fig. S1 Maximum likelihood phylogenetic tree for Bursera
species.
Table S1 List of species and GenBank accessions for Bursera
phylogenetic analysis
Table S2 List of species and GenBank accessions for eudicot
phylogenetic analysis
Table S3 Fossil calibration and constraints for eudicot dating
analysis
Table S4 Fossil calibration and constraints for Bursera dating
analysis
Table S5 List of Bursera species inserted in phylogenetic diversification analysis
Table S6 Fit of birth-death likelihood (BDL) diversification
models to Bursera
Methods S1 Detailed description of methods.
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