Testing geological models of evolution of the Isthmus of
Panama in a phylogenetic framework
CHRISTINE D. BACON1*, ANDR?S MORA2, WARREN L. WAGNER3 and
CARLOS A. JARAMILLO1
1Smithsonian Tropical Research Institute, Balboa, Anc?n, Republic of Panam?
2Instituto Colombiano del Petroleo, Ecopetrol, Piedecuesta, Colombia
3Department of Botany, Smithsonian Institution, MRC-166, PO Box 37012, Washington DC,
20013-7012, USA
Received 9 February 2012; revised 28 May 2012; accepted for publication 31 May 2012
The emergence and closure of the Isthmus of Panama had regional and global impacts that were rivalled by few
other Cenozoic geological events. The closure of the Central American Seaway and the rise of the Isthmus had
dramatic affects on climate and air and oceanic currents worldwide. Formation of the Isthmus also drove terrestrial
biotic interchange, ending the isolation of South America by permitting the mixing of its biota with that of North
and Central America. A dated phylogenetic tree of a well-sampled clade of palms in the tribe Trachycarpeae
(Copernicia, Pritchardia and Washingtonia) was used to conduct biogeographical analyses. Examination of the
timing of lineage dispersal from North into South America was performed and two contrasting temporal hypotheses
of the Isthmus formation were tested: occurrence in the Pliocene (c. 5 Mya to the present) or in the Miocene (prior
to c. 5 Mya). Copernicia is inferred to have dispersed through the Isthmus of Panama region into South America
and subsequently into the Caribbean, where it underwent a rapid radiation. Consistent with a geologically
older age for the Isthmus than previously understood, our results support recent geological and palaeobiological
data that suggest an early Oligocene to early Miocene model of evolution of the Isthmus of Panama. ? 2012 The
Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300.
ADDITIONAL KEYWORDS: Arecaceae ? biogeography ? Caribbean ? Central American Seaway ? Cuba ?
Hawaiian Islands ? Palmae ? phytogeography ? South America.
INTRODUCTION
The formation of the Isthmus of Panama is consid-
ered by physical scientists as one of the most impor-
tant geological events in Cenozoic history [last 60
million years (Mya); e.g. Graham, 2010]. The Isthmus
is a narrow strip of land that separates the Caribbean
Sea from the Pacific Ocean and links North and
Central America with South America. The closure of
the Central American Seaway (CAS) that separated
North and South America stopped the westward pal-
aeocurrent and all circulation between the Caribbean
Sea and the Pacific Ocean (Collins, Budd & Coates,
1996; Newkirk & Martin, 2009), forcing Caribbean
currents northeastward. The formation of the
Isthmus had an enormous impact on global climate
and, although controversial (Klocker, Prange &
Schulz, 2005; Molnar, 2008), the northeastern shift in
Caribbean currents has been hypothesized to have
played a fundamental role in the onset of Plio-
Pleistocene glaciations (Haug & Tiedemann, 1998;
Haug et al., 2001; Bartoli et al., 2005).
In addition to the climatic and oceanographic
effects, the closure of the Isthmus of Panama is also
considered to have been a defining event in the bio-
geography of the Americas (e.g. Gentry, 1982). New
land connections between North and South America
ended the ?splendid isolation? of South America
(Simpson, 1980) and facilitated the ?Great American
Biotic Exchange? (Stehli & Webb, 1985). The fossil
record of mammal fauna supports few migrations
across the Isthmus before the Late Pliocene and the*Corresponding author. E-mail: christinedbacon@gmail.com
bs_bs_banner
Botanical Journal of the Linnean Society, 2013, 171, 287?300. With 3 figures
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300 287
Pleistocene (Simpson, 1980; Stehli & Webb, 1985;
Graham, 1992; Burnham & Graham, 1999). For
plants, a recent meta-analysis has shown older trans-
CAS divergence times, implying a higher propensity
for dispersal than animals throughout the geological
period of Panamanian assembly (Cody et al., 2010)
and/or the presence of a dispersal corridor (approxi-
mating tectonic plates or stepping-stone islands
between North and South America). The combined
processes of plate disassembly and redistribution,
together with phases of global warming and cooling,
are thought to have afforded plants intermittent dis-
persal opportunities that could have contributed to
the direction of angiosperm diversification (Morley,
2003). In particular, long-distance dispersal has been
demonstrated to be the likely cause of many plant
distributions, including those in the Neotropics (e.g.
Dick, Abdul-Salim & Bermingham, 2003; Lavin et al.,
2004; S?rkinen et al., 2007).
Previous studies based on isotopic, geochemical and
fossil faunal data from sedimentary strata across
the Isthmus of Panama were inferred to indicate a
Pliocene emergence and closure of the Isthmus [c. 3
million years ago (Mya); Keigwin, 1978, 1982; Duque-
Caro, 1990; Coates et al., 1992, 2004; Collins et al.,
1996; Kameo & Sato, 2000; Beu, 2001; Newkirk &
Martin, 2009]. However, some of the evidence sup-
porting this Pliocene evolution model has alterna-
tively been interpreted to show no causal relationship
with Isthmus closure because these studies relied on
indirect evidence (geochemical, biological records)
assumed to be correlated with a Pliocene Isthmus
closure (e.g. Molnar, 2008). Indeed, previous results
are in contrast with a recently proposed model of
Isthmus formation based on new mapping, petro-
graphical, geochronological, palaeomagnetic and ther-
mochronological data, which infer that the Isthmus of
Panama region comprised primarily uplifted terres-
trial landscapes above sea level with some shallow
sea incursions from the late Eocene (c. 40?34 Mya;
Montes et al., 2012a, b) until the early Miocene
(c. 23?16 Mya; Farris et al., 2011). This Isthmus chain
implies that the likelihood of dispersal between North
and South America increased with the initiation of
collision between the easternmost tip of the Central
American Arc and northwestern South America, and
that emergence and closure of the Isthmus are much
older than previously recognized (CAS closure at
15 Mya; Montes et al., 2012a). This palaeogeographi-
cal configuration also greatly restricted the width of
the CAS during the late Oligocene to early Miocene
(200-km-wide sea gap at 25 Mya; Farris et al., 2011;
Montes et al., 2012a).
The integration of phylogenetic, molecular dating
and biogeographical methods can also be used to
reconstruct the evolutionary history of the Isthmus of
Panama, particularly when examining groups that
are keystone components of Neotropical forests
(e.g. Pennington, Richardson & Lavin, 2006). Palms
(Arecaceae) are among the most important and char-
acteristic components of tropical forests, particularly
in terms of species diversity and abundance of indi-
viduals (Kahn & de Granville, 1992; Phillips & Miller,
2002; Dransfield et al., 2008; Eiserhardt et al., 2011a).
Over 90% of palm species diversity is restricted to
tropical forests because of water- and energy-related
variables (Bjorholm et al., 2005; Kreft, Sommer &
Barthlott, 2006; Eiserhardt et al., 2011b) and because
of fundamental anatomical constraints that inhibit
palms from colonizing colder environments (Tomlin-
son, 2006). The rich fossil history of Arecaceae dates
back to the Cretaceous, and a recent family-wide
analysis of divergence times inferred that palms
have diversified in the tropical rainforest biome since
its mid-Cretaceous origin at northern latitudes
(Couvreur, Forest & Baker, 2011). Furthermore,
palms are present in the first record of Neotropical
forests (late Palaeocene Cerrej?n flora of Colombia;
Gomez-Navarro et al., 2009; Wing et al., 2009). Taken
together, palms are an excellent study system for
understanding the evolutionary history of the
Isthmus of Panama.
Within the palms, a monophyletic group of three
closely related genera of the palm tribe Trachy-
carpeae, Copernicia Mart., Pritchardia Seem. &
H.Wendl. and Washingtonia H.Wendl., are distributed
on both sides of the Isthmus region in North and
South America and comprise two explosive island
radiations, one in the Caribbean (Cuba and Hispa-
niola) and the other in the Pacific (Hawaiian Islands;
Fig. 1; Bacon, Baker & Simmons, 2012a; Bacon et al.,
2012b). A previous study has suggested that these
genera originated from North America and that
Copernicia lineages followed the Greater Antilles?
Aves Ridge (GAARlandia) land bridge to disperse
from the Caribbean to South America (Bacon et al.,
2012a). GAARlandia putatively comprised large,
closely spaced islands or possibly a continuous
peninsula that linked South America to the Greater
Antillean Islands in the Eocene?Oligocene transition
(35?33 Mya; Iturralde-Vinent & MacPhee, 1999; but
see Ali, 2012; Bayona et al., 2012). A GAARlandia
dispersal route for Copernicia was proposed because
the timing of dispersals predated a Pliocene Isthmus
of Panama formation (Bacon et al., 2012a), but the
recently proposed geologically older model of Isthmus
evolution merits examination as an alternative dis-
persal route.
Copernicia, Pritchardia and Washingtonia species
occur in dry, open savannas, deserts and areas prone
to seasonal flooding or, on Pacific islands, in wet
windward or dry leeward forests (Dransfield et al.,
288 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
2008) and are dispersed by small mammals and birds
(Henderson, 2002). Most wrens are insectivorous, but
the largest species (Campylorhynchus griseus) nests
and forages preferentially on Copernicia tectorum
Mart. and, although it has been shown to disperse
Copernicia seeds (Rabenold, 1990), dispersal does not
occur over long distances because of their nonmigra-
tory nature. Washingtonia spp. are also dispersed by
nonmigratory birds (Bullock, 1980) and by coyotes
(Cornett, 1985). In contrast, Pritchardia spp. disperse
across long distances along avian migratory routes of
various plovers (Pluvialis spp.) (e.g. Hodel, 2007).
These differences in dispersal capabilities, together
with the phylogenetic relationships among genera,
can be used to test the temporal biogeographical
history of the clade in the Neotropics.
To inset
Copernicia
Pritchardia
Washingtonia
Extant outgroups
Cenozoic fossil occurrences
Niue
Fiji
Solomons
Hawaii
Cook
Samoa
Australia
Pacific
Ocean
Tonga
Distributions
North America
South America
Caribbean Sea
Pacific Ocean
Isthmus
of
Panama
Figure 1. Map of the palm genera examined. Copernicia is distributed in Argentina, Brazil, Colombia, Cuba, Dominican
Republic, Haiti, Paraguay and Venezuela. Pritchardia is distributed in the Cook, Fiji, Hawaiian, Niue, Samoa, Solomon
and Tonga Islands. Washingtonia is distributed in the USA and Mexico. The Cenozoic fossil outgroups are based on
Sabalites fossil occurrences, which were derived from Read & Hickey (1972), Weber (1978), Harley (2006) and Dransfield
et al. (2008). Although the nomenclatural use of Sabalites does not unequivocally associate fossils with any extant genus
(e.g. Sabal), it is a good hypothesis of the palaeodistribution of the lineages examined.
ISTHMUS OF PANAMA BIOGEOGRAPHY 289
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
In this study, we investigate the origin and diver-
sification of Copernicia, Pritchardia and Washingto-
nia palms in space and time by estimating speciation
events under different biogeographical models. We
explore the biogeographical history of Copernicia and
the evolution of the Isthmus of Panama by testing
whether the timing of lineage dispersal occurred in
the Pliocene (5.25 Mya to the present; H1 sensu
Keigwin, 1978) or whether it occurred in the Miocene
(before 5.25 Mya; H2 sensu Montes et al., 2012a).
Elucidation of the timing of formation of the Isthmus
has major implications for the timing of biotic inter-
change between North and South America, and hence
for the elucidation of the diversification history of
Copernicia, Pritchardia and Washingtonia.
MATERIAL AND METHODS
PHYLOGENETIC ANALYSES AND ESTIMATION OF
DIVERGENCE TIMES
Species of Copernicia, Pritchardia and Washingtonia
and three outgroups representing other tribes of
Coryphoideae [Fig. 1; Cryosophila stauracantha
(Heynh.) R.J.Evans, Phoenix roebelenii O?Brian and
Sabal palmetto (Walter) Lodd. ex Schult. & Schult.f.]
were sequenced for three plastid and three nuclear
genes (Bacon et al., 2012a, b). Eighty per cent of
species were sampled, including 13 of the 22 species
of Copernicia, one of the two Washingtonia species
and all 26 currently recognized species of Pritchardia
(Hodel, 2007; Bacon et al., 2012b). Forty-three termi-
nals were included in the simultaneous analysis
(Kluge, 1989; Nixon & Carpenter, 1996). Preliminary
nucleotide alignments were obtained independently
for each of the six loci using default parameters in
MUSCLE v3.6 (Edgar, 2004) and manually adjusted
in MacClade v4.03 (Maddison & Maddison, 2001)
following Simmons (2004). Maximum parsimony (MP)
tree searches were conducted using 1000 random
addition tree bisection?reconnection (TBR) searches
in PAUP* v4.0b10 (Swofford, 2001) with a maximum
of ten trees held per replicate. Parsimony jackknife
(JK) analyses (Farris et al., 1996) were conducted
using PAUP* and 1000 replicates were performed
with 100 random addition TBR searches per replicate.
jModeltest v0.1.1 (Posada, 2008) was used to select
the best-fit model of sequence evolution for each data
matrix using the Akaike Information Criterion
(Akaike, 1974) without considering invariant-site
models, following Yang (2006). The data were parti-
tioned by locus to allow for variation in substitution
models and the analysis was run using the GTR + G
model of nucleotide substitution with four rate cat-
egories. Three iterations of Markov chain Monte
Carlo (MCMC) analysis were conducted with 50
million generations sampled every 1000th generation
to estimate the Bayesian topology in BEAST v1.6.2
(Drummond et al., 2006; Drummond & Rambaut,
2007). We estimated the divergence times using an
uncorrelated log-normal molecular clock model and
the Yule pure birth speciation model. We do not know
of any unambiguously identified fossils in Copernicia,
Pritchardia or Washingtonia, and we therefore used
two secondary calibration points obtained from a
family-level analysis based on four primary fossil
calibrations (Couvreur et al., 2011). Normally distrib-
uted priors have been shown to be most appropriate
for modelling secondary calibrations because they
reflect the uncertainty in age estimates (Ho, 2007; Ho
& Phillips, 2009). Normal distributions for both the
stem and crown nodes of Trachycarpeae were esti-
mated and the bounds on the prior reflect the 95%
credible interval of the constraints. The mean ages
were 54 and 34 Mya, respectively, sensu Couvreur
et al. (2011), and the standard deviations were set to
6 and 5 Mya, respectively, to capture the variation
estimated around the mean (71?38 and 47?23 Mya,
respectively, for the stem and crown nodes). The per-
formance of the separate analyses (convergence of
parameters, effective sample sizes) was assessed in
AWTY (Wilgenbusch, Warren & Swofford, 2004;
Nylander et al., 2008) and in Tracer v1.5 (Drummond
& Rambaut, 2007).
ANCESTRAL RANGE RECONSTRUCTION
A presence?absence matrix was built representing
the distribution of species (Fig. 1) in nine non-
overlapping areas that reflect the distributions
and endemism of genera, while at the same time
minimizing the total number of areas (Sanmart?n
& Ronquist, 2004): SU (southern USA: Arizona,
California, Florida, Georgia, North and South
Carolina); CM (Central America and Mexico); NW
(northwestern South America: Colombia and Ven-
ezuela); SC (south-central South America: Argentina
and Brazil); HA (Hispaniola: Dominican Republic and
Haiti); CU (Cuba); SP (south Pacific Islands: Cook,
Fiji, Niue, Samoa, Solomon and Tonga); HI (Hawaiian
Islands); and AS (Asia: China to Vietnam). Each
species was assigned to one or more of the
areas on the basis of its known current distribution
(Henderson, Galeano & Bernal, 1995; Hodel, 2007).
To reconstruct the historical biogeography of line-
ages and, in particular, to examine whether Coperni-
cia lineages followed a Central American (Isthmus of
Panama) or Caribbean (GAARlandia) dispersal route
into South America, we analysed an unconstrained
matrix in which dispersal among all regions was
equally probable using two methods: the Bayesian
statistical dispersal?vicariance analysis, as imple-
290 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
mented in Reconstruct Ancestral State in Phylogenies
(RASP in S-DIVA; Yu, Harris & He, 2010), and the
dispersal?extinction?cladogenesis likelihood model
(DEC), as implemented in Lagrange (build 20110117;
Ree et al., 2005; Ree & Smith, 2008). To take into
account the influence of phylogenetic uncertainty on
biogeographical inference, unconstrained ancestral
areas were optimized across a random sample of 1000
post-burn-in Bayesian trees from the dating analysis
in RASP. Relative frequencies of ancestral areas for
each node of the BEAST tree were computed by
counting all trees with a certain area uniquely
assigned to the node. Results that included the pro-
portion of ambiguous reconstructions (< 6% relative
probability) across the random sample were then
translated into pie charts by importing the estimated
relative frequencies from the RASP ?node view? into
Excel.
We also used the ultrametric tree generated by
BEAST to infer ancestral distributions with DEC
default parameters employing an unconstrained dis-
persal matrix, and compared it with two constrained
matrices, to test between alternative models on the
formation of the Isthmus of Panama. The constrained
matrices corresponded to Pliocene or Miocene palm
dispersal and were based on the fact that dispersal
probability increases as distance between areas
decreases (isolation by distance; e.g. MacArthur &
Wilson, 1967). Furthermore, the constraints restricted
dispersal between North and South America and the
Caribbean and Pacific basins, leaving the Asian and
south-central South American biogeographical regions
unconstrained. Constraints were defined by the mean
of the age ranges of the two hypotheses: 5.25 Mya
for the H1 Pliocene model (mean of 7.0 and 3.5 Mya)
and 21.5 Mya for the Miocene H2 model [mean of 35
and 8 Mya; timing of the 200-km CAS gap sensu
Farris et al. (2011) and Montes et al. (2012a)]. Differ-
ences between models were assessed by direct com-
parison of their respective log-likelihoods using
the conventional cut-off value of two log-likelihood
units following Ree et al. (2005). Palms do not require
strict over-land dispersal or, in this case, completion
of the Panamanian land bridge, but because of the
dispersal capabilities of Copernicia, long-distance
over-water events are unlikely. We therefore formed
discrete hypotheses to allow for comparison and to
emphasize two distinct temporal scenarios of isthmian
evolution.
Two iterations of hypothesis testing using biogeo-
graphical constraints were performed. In the ?strict?
analysis, the H1 matrix was constrained to only allow
dispersal of palms from North America (SU and CM)
across the Isthmus to South America (NW) from 7 to
0 Mya and through the CAS either to the Pacific (SP
and HI) or Caribbean basins (CU and HA) from 20.00
to 5.25 Mya. We compared the likelihoods for H1 with
H2, where the matrix was constrained to only allow
dispersal across the Isthmus between 35 and 8 Mya
and through the CAS from 50 to 21.5 Mya. In the
?relaxed? analysis, the H1 matrix allowed for low
dispersal (0.25) into South America from 20.00 to
5.25 Mya and the H2 matrix allowed a medium rate of
dispersal (0.5) into South America from 7 to 0 Mya.
RESULTS
PHYLOGENETIC RELATIONSHIPS
Phylogenetic analyses of 6843 bp of nuclear and
plastid data using parsimony and Bayesian methods
were consistent with the maximum likelihood topol-
ogy, but differed from the Bayesian topology, pre-
sented in Bacon et al. (2012a; figs 2, 4 versus fig. 5)
with respect to the placement of Washingtonia.
Eleven nodes had relatively poor support values, but
they corresponded to lineages within recent and rapid
island radiations (Supporting Information, Fig. S1).
Each genus was highly supported [posterior probabil-
ity (PP) = 1; JK = 100%] as monophyletic, as were
major clades within genera, such as South American
Copernicia, south-central South American Copernicia,
Hispaniolan Copernicia, Cuban Copernicia, south
Pacific Pritchardia and Hawaiian Pritchardia. Many
of the Pritchardia clades endemic to particular
Hawaiian Islands were also resolved as highly sup-
ported monophyletic biogeographical groups (PP = 1
for Kaua?i, Maui Nui and Hawaiian clades; Fig. 2).
TEMPORAL RANGE EVOLUTION ACROSS THE ISTHMUS
OF PANAMA
Each of the three iterations of 50 million generations
resulted in high effective sample sizes (ESSs) (> 500)
and convergence of parameters (?Compare? function in
AWTY), and 10% of the sampled trees were subse-
quently treated as burn-in and removed. For all four
data partitions (plastid, CISP4, CISP5, RPB2), the
rate of covariance was centred on zero, which can be
interpreted as a lack of evidence for rate autocorre-
lation among lineages (Drummond & Rambaut,
2007). The estimated ages of the major clades are
given in Table 1.
The estimation of ancestral ranges was consistent
between likelihood (DEC) and Bayesian (RASP)
unconstrained inferences. Relative frequencies from
the RASP analysis across the sample of posterior
trees (Fig. 2) reconstructed the ancestral area of
Copernicia, Pritchardia and Washingtonia as prima-
rily distributed in the southern USA, but a few topolo-
gies supported a Central America + Mexico ancestral
area or a combination of the two regions. The ances-
tral area of the Copernicia and Pritchardia clade was
ISTHMUS OF PANAMA BIOGEOGRAPHY 291
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
inferred in the southern USA. The area reconstruc-
tion suggests that Copernicia subsequently dispersed
across the Isthmus of Panama region into northwest-
ern South America, with lineages reaching the Car-
ibbean only after the colonization of South America.
Comparison of H1 and H2 across the two iterations
of DEC constrained analyses resulted in four biogeo-
graphical scenarios that were within two log-
likelihood units of one another (Table 2). The best
estimate from the comparison of log-likelihood values
was that of a relaxed constraint on a Miocene (H2)
colonization of South America across the Isthmus of
Panama. This scenario was 0.35 log-likelihood units
lower than the unconstrained and 0.22 units lower
than the relaxed H1 results. Range evolution infer-
ences under the relaxed H2 constraint exhibited less
uncertainty in range reconstructions than did the
strict or unconstrained models, showing that the
relaxed model fit the data better.
The likelihood-based and Bayesian biogeographical
reconstructions are highly congruent and allow for a
most likely hypothesis of lineage diversification and
range evolution in Copernicia, Pritchardia and Wash-
ingtonia (Fig. 3): the ancestral area of the three palm
genera was located in the southern USA (SU) around
33.5 Mya with subsequent divergence of Copernicia
and Pritchardia lineages also occurring in SU around
31 Mya. Copernicia dispersed into northwestern
South America between 31 and 16.3 Mya, and then to
the Caribbean islands between 16.3 and 5.5 Mya,
whereas Pritchardia dispersed to the Pacific islands
between 31 and 9.1 Mya (Table 1), with both genera
Figure 2. Bayesian topology derived from three iterations of a 50-million-generation Markov chain Monte Carlo (MCMC)
search. Branch support values for the nodes of interest were all resolved with a Bayesian posterior probability (PP) of 1.0.
Nodes of interest that were resolved with less than 100% jackknife (JK) on the maximum parsimony (MP) strict consensus
tree are beneath the respective branches, and * indicates relationships that were not present in the strict consensus. Pie
charts of the relative frequencies of ancestral ranges at the nodes of interest are derived from 1000 posterior trees in
Reconstruct Ancestral State in Phylogenies (RASP) and the grey stars indicate the two calibration points.
292 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
subsequently undergoing rapid radiations in Cuba (17
species at 4.45 Mya; Table 1) and the Hawaiian
Islands (23 species at 4.17 Mya), respectively.
DISCUSSION
Robust molecular age estimates and biogeographical
analysis of Copernicia, Pritchardia and Washingtonia
were used to examine the likely dispersal route of
Copernicia from North to South America and, subse-
quently, to infer the timing of palm dispersal and
diversification across the Panamanian Isthmus and to
the Caribbean and Pacific oceanic basins. Divergence
time estimations are consistent with a general
pattern of angiosperm colonization of Hawaiian
Islands occurring at approximately 5 Mya (~4 Mya in
Pritchardia, Table 1; e.g. Baldwin & Sanderson, 1998;
Frajman, Eggens & Oxelman, 2009; Bacon et al.,
2012a), which has been attributed to the emergence of
the extant volcanic islands, and also with the timing
of the formation of the distinct components of Cuba
into a single island terrain (Pliocene Cuban Coperni-
cia radiation; Iturralde-Vinent & MacPhee, 1999;
Graham, 2003; MacPhee, Iturralde-Vinent & Gaffney,
2003). Our results support a Copernicia dispersal
event from North America via the Isthmus of Panama
region into South America. Our results are also
consistent with an early Oligocene to early Miocene
formation of the Isthmus, which is older than tradi-
tionally understood and is further supported by
recent geological and palaeobiological data in the
proposal of a revised tectonic model of evolution of the
Isthmus of Panama.
TESTING ALTERNATIVE HYPOTHESES ON THE
FORMATION OF THE ISTHMUS OF PANAMA IN
TRACHYCARPEAE PALMS
After identifying a Copernicia dispersal route through
the Isthmus of Panama region, we used a likelihood
approach to test two alternative hypotheses. The first
hypothesis (H1) was consistent with previous studies
showing Pliocene dispersal across the Isthmus (here
defined as a mean age of 5.25 Mya; but see Cody
et al., 2010). The second hypothesis (H2) tested a
revised tectonic model of Isthmus evolution proposed
by Farris et al. (2011) and Montes et al. (2012a, b),
where land emergence and subsequent formation of
the Isthmus of Panama allowed for earlier biotic
exchange (late Oligocene to early Miocene; here
defined as a mean age of 21.5 Mya).
The phylogenetic analysis suggests a biogeographi-
cal disjunction between the Caribbean and Pacific
basins. Sister groups that are disjunct between the
Caribbean and Pacific are apparently rare and have
been correlated with the formation of the Isthmus
(Namoff et al., 2010), including the effects on global
climate and air and oceanic currents. In angiosperms,
this disjunction is exemplified in Darwiniothamnus
Harling and Erigeron L. (Andrus et al., 2009), Jac-
quemontia Choisy (Namoff et al., 2010), Fitchia
Hook.f, Oparanthus Sherff, Narvalina Cass. and
Selleophytum Urb. (Mort et al., 2008), Siemensia Urb.
(Motley, Wurdack & Delprete, 2005), and as found
here in Copernicia and Pritchardia. These genera of
Trachycarpeae originated in North America between
41 and 25 Mya (Table 1) and lineages dispersed both
across the Isthmus of Panama and to Pacific islands.
Table 1. Crown and stem node mean and highest posterior density estimations in millions of years ago (Mya) for clades
of interest based on two calibration points
Clade
Stem Crown
Mean Upper Lower Mean Upper Lower
Pritchardia 31.04 38.98 23.13 9.12 13.26 5.30
South Pacific Pritchardia 9.12 13.26 5.30 7.34 11.02 4.12
Hawaiian Islands Pritchardia 9.12 13.26 5.30 4.17 6.35 2.19
Kaua?i Pritchardia 2.84 4.28 1.55 2.28 3.62 1.09
Maui Nui Pritchardia * * * 1.57 2.63 0.66
Hawai?i Pritchardia * * * 1.43 2.44 0.55
Copernicia 31.04 38.98 23.13 16.34 22.11 10.65
Central-east South America Copernicia 9.66 14.17 5.53 4.99 8.02 2.36
Hispaniola Copernicia 5.55 8.26 3.07 2.33 4.23 0.73
Cuban Copernicia 5.55 8.26 3.07 4.45 6.68 2.49
Copernicia + Pritchardia 33.49 41.65 25.54 31.04 38.98 23.13
Copernicia + Pritchardia + Washingtonia 49.80 60.50 39.28 33.49 41.65 25.54
*Nodes supported by posterior probabilities lower than 0.50.
ISTHMUS OF PANAMA BIOGEOGRAPHY 293
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
The biogeographical disjunction between Copernicia
and Pritchardia evolved between 31 and 9.1 Mya and
implies long-distance dispersal of Pritchardia by
migratory birds from North America to the Hawaiian
Islands and therefore may be unrelated to Isthmus
formation, but this temporal framework corresponds
to increased constriction of the CAS as inferred from
geological and palaeobiological data (early Oligocene
to early Miocene; Montes et al., 2012b). CAS closure
not only rerouted air and west to east oceanic
currents (Collins et al., 1996), but potentially avian
migratory (and palm dispersal) routes by forming
emergent terrestrial proto-isthmus breeding and
feeding grounds that mitigated against further
dispersal.
Our results from divergence time and ancestral
range reconstructions are consistent with an early
Oligocene to early Miocene model of evolution for the
Isthmus of Panama. In this model, dispersal between
North and South America (Table 2) occurred between
31 and 16.3 Mya. Considering these scenarios in rela-
tion to current species richness, it is striking that the
North American ancestor lineage apparently did not
diversify in a continental setting. Two Washingtonia
spp. and three non-Caribbean Copernicia spp. gave
rise to much more diverse island lineages: 19 Carib-
bean island Copernicia spp. and 26 South Pacific
island Pritchardia spp. The lack of continental diver-
sification is interesting given that there was
no dispersal barrier into newly available South
American niches, as seen by Copernicia lineages that
apparently failed to diversify after colonizing north-
western South America by at least 16 Mya, unlike
other angiosperms [e.g. Guatteria Ruiz & Pav. (Erkens
Table 2. Constraints implemented in dispersal?extinction?cladogenesis likelihood model (DEC) analyses to test between
the alternative models of Isthmus of Panama formation
H1 H2
NW SP HI HA CU NW SP HI HA CU
Strict
0?5.25 Mya
SU 1 0 0 0 0 0 0 0 0 0
CM 1 0 0 0 0 0 0 0 0 0
5.25?21.5 Mya
SU 0 1 1 1 1 1 0 0 0 0
CM 0 1 1 1 1 1 0 0 0 0
21.5?50 Mya
SU 0 0 0 0 0 0 1 1 1 1
CM 0 0 0 0 0 0 1 1 1 1
?ln L 42.76 42.47
Relaxed
0?5.25 Mya
SU 1 0 0 0 0 0.5 0 0 0 0
CM 1 0 0 0 0 0.5 0 0 0 0
5.25?21.5 Mya
SU 0.25 1 1 1 1 1 0.25 0.25 0.25 0.25
CM 0.25 1 1 1 1 1 0.25 0.25 0.25 0.25
21.5?50 Mya
SU 0 0.5 0.5 0.5 0.5 0 1 1 1 1
CM 0 0.5 0.5 0.5 0.5 0 1 1 1 1
?ln L 42.54 42.32
All other biogeographical regions not listed in the constraint matrix below were left unconstrained with a dispersal
capability of ?1?. The strict analysis reduced dispersal to zero and prohibited movement between two areas during
particular time periods, whereas the relaxed analysis reduced dispersal to 0.25 and 0.5 to allow for lower levels of
dispersal. Constrained biogeographical areas are abbreviated as southern USA (SU), Central America and Mexico (CM),
northwestern South America (NW), south Pacific Islands (SP), Hawaiian Islands (HI), Hispaniola (HA) and Cuba (CU).
The three time periods constrained in Lagrange were 5.25 Mya (mean of 7?3.5 Mya sensu Keigwin, 1978), 21.5 Mya (mean
of 35?8 Mya sensu Montes et al., 2012a) and 50 Mya (the stem node of the phylogeny estimated). Global maximum
likelihood values at the root nodes (as measured by ?ln L) are used to test amongst the two constrained and unconstrained
(?ln L of 42.67) likelihood analyses.
294 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
et al., 2007); Inga Mill. (Richardson et al., 2001)] or
other groups [e.g. tanager birds (Weir, Bermingham &
Schluter, 2009); North American mammals (Kirby,
Jones & MacFadden, 2008)].
A REVISED MODEL OF EVOLUTION OF THE ISTHMUS
OF PANAMA: ISSUES AND FUTURE PROSPECTS
Despite the caveats involved in studies employing
secondary calibration and a lack of biogeographical
algorithms that take into account rate differences
amongst regions in speciation, extinction or range
evolution (Goldberg, Lancanster & Ree, 2011), our
inferences from phylogenetic, divergence time and
biogeographical analyses are consistent with an early
Oligocene to early Miocene evolution of the Isthmus of
Panama, as suggested previously by Farris et al.
(2011). We did not find support for Eocene evolution
as proposed by Montes et al. (2012a, b), in these palm
lineages, perhaps because estimates based on fossil
data can only provide minimum ages (e.g. Ho, 2007).
Our data on Copernicia and Pritchardia support a
divergence between the two clades showing east?west
(31?9.1 Mya) and north?south (31?16 Mya) disjunc-
tions, consistent with the idea of an earlier formation
of the Isthmus of Panama.
These results together with a geologically older
formation of the Isthmus of Panama are consistent
with other studies on Neotropical palms (Cuenca,
Asmussen-Lange & Borchsenius, 2008; Roncal et al.,
Pacific O
cean
C
aribbean S
ea
S
A
N
C
A
49.8
33.5
31.0
16.3
9.6
5.5
9.1
40.9
Biotic interchange
between North and
South America
20 Mya 10 Mya40 Mya
SU SU
SP
SC
NW
SU
SU
SP
NW
NW
HA
50                                40                                  30                                20                                 10                                  0 Mya
EOCENE                                    OLIGOCENE                                  MIOCENE                        PLI     PLE
Figure 3. The most likely hypothesis of biogeographical events and diversification of Caribbean, Pacific, South American
(SA) and North and Central American (NCA) lineages. Ancestral nodes are plotted against hypothetical palaeomaps of the
Isthmus of Panama, where the shading darkens with the probability of biotic exchange between North and South
America. Inferred dispersal events (arrows) and most likely ancestral areas are also indicated at the nodes of interest.
HA, Hispaniola; NW, northwestern South America; PLE, Pleistocene; PLI, Pliocene; SC, south-central South America; SP,
south Pacific; SU, southern USA. The grey gradient indicates the timing of palm dispersal across the Isthmus of Panama.
ISTHMUS OF PANAMA BIOGEOGRAPHY 295
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
2010, 2011, 2012; Bacon et al., 2012a), where disper-
sal events from North to South America predate a
Pliocene model of Isthmus of Panama formation.
Excluding studies that used the Isthmus as a calibra-
tion point, which cannot test for the effects of closure,
other phylogenetic studies are consistent with a
model of Isthmus formation that is older than the
Pliocene [e.g. other angiosperms (Cody et al., 2010),
freshwater fish (Bermingham & Martin, 1998) and
salt-water-intolerant frogs (Weight et al., 2005; Pinto-
S?nchez et al., 2012)].
Support for an older early Oligocene to early
Miocene model of Isthmus of Panama formation
also derives from the palaeobiological record. Land
mammal fossil occurrences have been shown to
require a continuous land connection of Panama with
North America by the early Miocene (Whitmore &
Stewart, 1965; Kirby & MacFadden, 2005; Kirby
et al., 2008). Fossil benthic foraminifera also indicate
an effective biogeographical barrier between Carib-
bean and Pacific surface water in the middle to late
Miocene (Collins et al., 1996). Furthermore, regional
palaeogeographical reconstructions account for a
narrow gap, or the complete absence of a gap,
between Central America and northwest South
America in the Neogene (Wadge & Burke, 1983;
Pindell & Kennan, 2009). Despite this evidence, other
data remain to be explained, such as the dramatically
low mitochondrial rate of mutation required to
explain marine geminate sister species formed by a
much older Isthmus of Panama vicariant event (e.g.
Lessios, 2008). To this end, more dated phylogenetic
analysis of Neotropical groups and refined meta-
analyses examining biotic interchange in both marine
and terrestrial organisms are needed (C. D. Bacon,
C. Jaramillo & A. Antonelli, unpubl. data, but see
Lessios, 2008; Weir et al., 2009; Cody et al., 2010;
Smith & Klicka, 2010).
The implications of a geologically older model of the
emergence and formation of the Isthmus of Panama
are wide ranging and include biological, climatic,
oceanic and tectonic factors. Biologically, an early
Oligocene to early Miocene (31?16.3 Mya) land con-
nection between Central America and South America
through the Isthmus of Panama implies that the lack
of interchange in land mammals across the Isthmus
until the late Pliocene?early Pleistocene may have
been the result of a wet and hot climate in northern
South America that stalled mammal dispersal until
the formation of northern ice sheets and the evolution
of savanna-like environments in Panama and north-
ern South America (Molnar, 2008; Montes et al.,
2012a). In contrast, if a phylogenetic niche conserva-
tism hypothesis is asserted, the dispersal of dry-
adapted Copernicia palms that are resistant to
intermittent flooding may indicate the presence of
savanna-type ecosystems at least in the Miocene, but
further studies of biotic interchange among charac-
teristic savanna species are needed to shed further
light on the palaeoenvironment in the region.
An early Oligocene to early Miocene Isthmus for-
mation and land connection between Central and
South America are also significant in the context of
mountain building in the Andes. From the central
(Oncken et al., 2006) to the northern (Mora et al.,
2010) Andes, it has been suggested that deformation
reached most of the present-day extension of the
modern Andes in the late Oligocene to early Miocene.
Farris et al. (2011) suggested the late Oligocene to
early Miocene to be an important episode of deforma-
tion in Panama. It appears likely that the faster
westward South American drift, which is thought to
be responsible for orogenesis in the Andes (Silver,
Russo & Lithgow-Bertelloni, 1998; Oncken et al.,
2006; Mora et al., 2010; Husson, Conrad & Faccenna,
2012), also influenced the late Oligocene to early
Miocene closure of the CAS. Our data are robust to
these suggestions because the age for Isthmus
formation is coeval with important processes in
the Andes. The refined inference of the formation of
the Isthmus of Panama also has implications for the
understanding of Andean biogeography. Previous
studies of Andean lineages lacked unique and testable
predictions that facilitated such investigations (e.g.
Brumfield & Capparella, 1996) because events and
processes causing Andean biogeographical and tem-
poral patterns were thought to occur at overlapping
time intervals (Pleistocene climatic shifts, uplift of
the eastern cordillera of the northern Andes and the
completion of the Isthmus of Panama; Pennington &
Dick, 2010). Our results, together with the new tec-
tonic model of evolution in the Isthmus of Panama
proposed by Farris et al. (2011) and Montes et al.
(2012a, b), allow for the disentanglement of the effects
of the Isthmus closure and Pleistocene glacial cycles.
ACKNOWLEDGEMENTS
We acknowledge financial support from Ecopetrol
(?Cronolog?a de la Deformaci?n en las Cuencas
Subandinas? Project), the Montgomery Botanical
Center, the National Tropical Botanical Garden and
the Smithsonian Institution. We thank A. Antonelli
for inviting us to submit a paper to this special
issue on Neotropical Plant Evolution, T. L. P. Cou-
vreur for comments on an early draft, F. Alda, E.
Bermingham, D. A. Clague, H. A. Lessios, J. P. Price,
J. G. R. Romero, J. Roncal and J. D. C. S?nchez for
discussion, and the Associate Editor and two anony-
mous reviewers for suggestions that improved the
manuscript.
296 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
REFERENCES
Akaike H. 1974. A new look at the statistical model identi-
fication. IEEE Transactions on Automatic Control 19: 716?
723.
Ali JR. 2012. Colonizing the Caribbean: is the GAARlandia
land-bridge hypothesis gaining a foothold? Journal of
Biogeography 39: 431?433.
Andrus N, Tye A, Nesom G, Bogler D, Lewis C, Jaramillo
P, Fransisco-Ortega J. 2009. Phylogenetics of Darwini-
othamnus (Asteraceae: Astereae) ? molecular evidence for
multiple origins in the endemic flora of the Gal?pagos
Islands. Journal of Biogeography 36: 1055?1069.
Bacon CD, Baker WJ, Simmons MP. 2012a. Miocene
dispersal drives island radiations in the palm tribe
Trachycarpeae (Arecaceae). Systematic Biology 61: 426?
442.
Bacon CD, McKenna MJ, Simmons MP, Wagner WL.
2012b. Evaluating multiple criteria for species delimitation:
an empirical example using Hawaiian palms (Arecace-
ae:Palmae). BMC Evolutionary Biology 12: e23.
Baldwin BG, Sanderson MJ. 1998. Age and rate of
diversification of the Hawaiian silversword alliance (Com-
positae). Proceedings of the National Academy of Sciences,
USA 95: 9402?9406.
Bartoli G, Sarthein M, Weinelt M, Erlenkeuser H,
Garbe-Sch?nberg D, Lea DW. 2005. Final closure of
Panama and the onset of Northern Hemisphere glaciation.
Earth and Planetary Science Letters 237: 33?44.
Bayona G, Cardona A, Jaramillo C, Mora A, Montes C,
Valencia V, Ayala C, Montenegro O, Iba?ez-Meija M.
2012. Early Paleogene magmatism in the northern
Andes: insights on the effects of oceanic plateau?continent
convergence. Earth and Planetary Science Letters 331:
97?111.
Bermingham E, Martin AP. 1998. Comparative mtDNA
phylogeography of neotropical freshwater fishes: testing
shared history to infer the evolutionary landscape of lower
Central America. Molecular Ecology 7: 499?517.
Beu AG. 2001. Gradual Miocene to Pleistocene uplift of the
Central American Isthmus: evidence from tropical American
tonnoidean gastropods. Journal of Paleontology 75: 706?
720.
Bjorholm S, Svenning J-C, Skov F, Balslev H. 2005.
Environmental and spatial controls of palm (Arecaceae)
species richness across the Americas. Global Ecology and
Biogeography 14: 423?429.
Brumfield RT, Capparella AP. 1996. Historical diversifica-
tion of birds in northwestern South America: a molecular
perspective on the role of vicariant events. Evolution 50:
1607?1624.
Bullock SH. 1980. Dispersal of a desert fan palm by oppor-
tunistic frugivores. Principes 24: 29?32.
Burnham RJ, Graham A. 1999. The history of Neotropical
vegetation: new developments and status. Annals of the
Missouri Botanical Garden 86: 546?589.
Coates AG, Collins LS, Aubry M-P, Berggren WA. 2004.
The geology of the Darien, Panama, and the late Miocene?
Pliocene collision of the Panama arc with northwestern
South America. Geological Society of America Bulletin 116:
1327?1344.
Coates AG, Jackson JBC, Collins LS, Cronin TM,
Dowsett HJ, Bybell LM, Jung P, Obando JA. 1992.
Closure of the Isthmus of Panama; the near-shore marine
record of Costa Rica and western Panama. Geological
Society of America Bulletin 104: 814?828.
Cody S, Richardson JE, Rull V, Ellis C, Pennington RT.
2010. The Great American Biotic Interchange revisited.
Ecography 33: 326?332.
Collins LS, Budd AF, Coates AG. 1996. Earliest evolution
associated with closure of the Tropical American Seaway.
Proceedings of the National Academy of Sciences, USA 93:
6069?6072.
Cornett JW. 1985. Germination of Washingtonia filifera
seeds by coyotes. Principes 29: 19.
Couvreur TLP, Forest F, Baker WJ. 2011. Origin and
global diversification patterns of tropical rain forests:
inferences from a complete genus-level phylogeny of palms.
BMC Biology 9: e344.
Cuenca A, Asmussen-Lange CB, Borchsenius F. 2008. A
dated phylogeny of the palm tribe Chamaedoreeae supports
Eocene dispersal between Africa, North and South America.
Molecular Phylogenetics and Evolution 46: 760?775.
Dick CW, Abdul-Salim K, Bermingham E. 2003. Molecular
systematic analysis reveals cryptic Tertiary diversification
of a widespread tropical rain forest tree. The American
Naturalist 162: 691?703.
Dransfield J, Uhl NW, Asmussen CB, Baker WJ, Harley
MM, Lewis CE. 2008. Genera palmarum: the evolution and
classification of palms. Kew: Kew Publishing.
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006.
Relaxed phylogenetics and dating with confidence. PLoS
Biology 4: e88.
Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evo-
lutionary analysis by sampling trees. BMC Evolutionary
Biology 7: e214.
Duque-Caro H. 1990. Neogene stratigraphy, paleoceanogra-
phy and paleobiogeography in northwest South America and
the evolution of the Panama Seaway. Palaeogeography,
Palaeoclimatology, Palaeoecology 77: S203?S234.
Edgar RC. 2004. MUSCLE: multiple sequence alignment
with high accuracy and high throughput. Nucleic Acids
Research 32: 1792?1797.
Eiserhardt WL, Svenning J-C, Kissling WD, Balslev H.
2011a. Geographical ecology of the palms (Arecaceae):
determinants of diversity and distributions across spatial
scales. Annals of Botany 108: 1391?1406.
Eiserhardt WL, Bjorholm S, Svenning J-C, Rangel TF,
Balslev H. 2011b. Testing the water-energy theory on
American palms (Arecaceae) using geographically weighted
regression. PLoS ONE 6: e27027.
Erkens RHJ, Chatrou LW, Maas JW, van der Niet T,
Savolainen V. 2007. A rapid diversification of rainforest
trees (Guatteria; Annonaceae) following dispersal from
Central into South America. Molecular Phylogenetics and
Evolution 44: 399?411.
ISTHMUS OF PANAMA BIOGEOGRAPHY 297
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
Farris DW, Jaramillo C, Bayona G, Restrepo-Moreno
SA, Montes C, Cardona A, Mora A, Speakman RJ,
Glascock MD, Valencia V. 2011. Fracturing of the Pana-
manian Isthmus during initial collision with South America.
Geology 39: 1007?1010.
Farris JS, Albert VA, K?llersj? M, Lipscomb D, Kluge
AG. 1996. Parsimony jackknifing outperforms neighbor-
joining. Cladistics 12: 99?124.
Frajman B, Eggens F, Oxelman B. 2009. Hybrid origins
and homoploid reticulate evolution within Heliosperma
(Silenaeae, Caryophyllaceae) ? a multigene approach with
relative dating. Systematic Biology 58: 328?345.
Gentry AH. 1982. Neotropical floristic diversity: phytogeo-
graphical connections between Central and South America,
Pleistocene climatic fluctuations, or an accident of the
Andean orogeny? Annals of the Missouri Botanical Garden
69: 557?593.
Goldberg EE, Lancanster LT, Ree RH. 2011. Phylogenetic
inference of reciprocal effects between geographic range
evolution and diversification. Systematic Biology 60: 451?
465.
Gomez-Navarro C, Jaramillo C, Herrera F, Wing SL,
Callejas R. 2009. Palms (Arecaceae) from a Paleocene
rainforest in northern Colombia. American Journal of
Botany 96: 1300?1312.
Graham A. 1992. Utilisation of the Isthmian landbridge
during the Cenozoic ? palaeobotanical evidence for timing,
and the selective influence of altitudes and climate. Review
of Palaeobotany and Palynology 72: 119?128.
Graham A. 2003. Geohistory models and Cenozoic paleoen-
vironments of the Caribbean region. Systematic Botany 28:
378?386.
Graham A. 2010. Late Cretaceous and Cenozoic history of
Latin American vegetation and terrestrial environments. St.
Louis, MO: Missouri Botanical Garden Press.
Harley MM. 2006. A summary of fossil records for Arecaceae.
Botanical Journal of the Linnean Society 151: 39?67.
Haug GH, Tiedemann R. 1998. Effect of the formation of the
Isthmus of Panama on Atlantic thermohaline circulation.
Nature 393: 673?676.
Haug GH, Tiedemann R, Zahn R, Ravelo AC. 2001. Role
of Panama uplift on oceanic freshwater balance. Geology 29:
207?210.
Henderson A. 2002. Evolution and ecology of palms. Bronx,
NY: The New York Botanical Garden Press.
Henderson A, Galeano G, Bernal R. 1995. Field guide to
the palms of the Americas. Princeton, NJ: Princeton Uni-
versity Press.
Ho SYW. 2007. Calibrating molecular estimates of substitu-
tion rates and divergence times in birds. Journal of Avian
Biology 38: 409?414.
Ho SYW, Phillips MJ. 2009. Accounting for calibration
uncertainty in phylogenetic estimates of evolutionary diver-
gence times. Systematic Biology 58: 367?380.
Hodel DR. 2007. A review of the genus Pritchardia. Palms
51S: S1?S53.
Husson L, Conrad CP, Faccenna C. 2012. Plate motions,
Andean orogeny, and volcanism above the South Atlantic
convection cell. Earth and Planetary Science Letters 317:
126?135.
Iturralde-Vinent MA, MacPhee RDE. 1999. Paleogeogra-
phy of the Caribbean region: implications for Cenozoic bio-
geography. Bulletin of the American Museum of Natural
History 238: 1?95.
Kahn F, de Granville J-J. 1992. Palms in forest ecosystems
of Amazonia. Berlin: Springer-Verlag.
Kameo K, Sato T. 2000. Biogeography of Neogene calcareous
nannofossils in the Caribbean and the eastern equatorial
Pacific ? floral response to the emergence of the Isthmus of
Panama. Marine Micropaleontology 39: 201?218.
Keigwin LD. 1978. Pliocene closing of the Isthmus of
Panama, based on biostratigraphic evidence from nearby
Pacific Ocean and Caribbean Sea cores. Geology 6: 630?
634.
Keigwin LD. 1982. Isotopic paleoceanography of the Carib-
bean and east Pacific; role of Panama uplift in the late
Neogene time. Science 217: 350?353.
Kirby MX, Jones DS, MacFadden B. 2008. Lower Miocene
stratigraphy along the Panama Canal and its bearing on the
Central American Peninsula. PLoS ONE 3: e14.
Kirby MX, MacFadden B. 2005. Was southern Central
America an archipelago or a peninsula in the middle
Miocene? A test using land-mammal body size. Palaeogeog-
raphy, Palaeoclimatology, Palaeoecology 228: 193?202.
Klocker A, Prange M, Schulz M. 2005. Testing the influ-
ence of the Central American Seaway on orbitally forced
Northern Hemisphere glaciation. Geophysical Research
Letters 32: 1?4.
Kluge AG. 1989. A concern for evidence and a phylogenetic
hypothesis for relationships among Epicrates (Boideae,
Serpentes). Systematic Zoology 38: 7?25.
Kreft H, Sommer JH, Barthlott W. 2006. The significance
of geographic range size for spatial diversity patterns in
neotropical palms. Ecography 29: 1?30.
Lavin M, Schrire BD, Lewis G, Pennington RT, Delgado-
Salinas A, Thulin M, Hughes CE, Beyra-Matos A,
Wojciechowski MF. 2004. Metacommunity processes
rather than continental tectonic history better explain geo-
graphically structured phylogenies in legumes. Philosophi-
cal Transactions of the Royal Society, Biological Series 359:
1509?1522.
Lessios HA. 2008. The Great American Schism: divergence of
marine organisms after the rise of the Central American
Isthmus. Annual Review of Ecology, Evolution, and System-
atics 39: 63?91.
MacArthur RH, Wilson EO. 1967. The theory of
island biogeography. Princeton, NJ: Princeton University
Press.
MacPhee RDE, Iturralde-Vinent MA, Gaffney ES. 2003.
Domo de Zaza, and early Miocene vertebrate locality in
south-central Cuba, with notes on the tectonic evolution of
Puerto Rico and the Mona Passage. American Museum
Novitates 3394: 1?42.
Maddison DR, Maddison WP. 2001. Macclade: analysis of
phylogeny and character evolution version 4.03. Sunderland,
MA: Sinauer Associates.
298 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
Molnar P. 2008. Closing of the Central American Seaway and
the Ice Age: a critical review. Paleooceanography 23: DOI:
10.1029/2007PA001574.
Montes C, Cardona A, McFadden R, Mor?n SE, Silva CA,
Restrepo-Moreno S, Ramir?z DA, Hoyos N, Farris D,
Bayona GA, Jaramillo CA, Valencia V, Bryan J, Flores
JA. 2012a. Evidence for middle Eocene and younger land
emergence in Central Panama: implications for Isthmus
closure. Geological Society of America Bulletin 124: DOI:
10.1130/B30528.1.
Montes C, Bayona GA, Cardona A, Buchs DM, Silva CA,
Mor?n SE, Hoyos N, Ramir?z DA, Jaramillo CA,
Valencia V. 2012b. Arc?continent collision and orocline
formation: closing of the Central American Seaway.
Journal of Geophysical Research 117: DOI: 10.1029/
2011JB008959.
Mora A, Horton B, Mesa A, Rubiano J, Ketchum R,
Parra M, Blanco M, Garc?a D, Stockli D. 2010. Migra-
tion of Cenozoic deformation in the Eastern Cordillera of
Colombia interpreted from fission track results and struc-
tural relationships: implications for petroleum systems.
American Association of Petroleum Geologists Bulletin 94:
1543?1580.
Morley RJ. 2003. Interplate dispersal paths for megathermal
angiosperms. Perspectives in Plant Ecology, Evolution and
Systematics 6: 5?20.
Mort ME, Randle CP, Kimball RT, Tadesse M, Crawford
DJ. 2008. Phylogeny of Coreopsidae (Asteraceae) inferred
from nuclear and plastid DNA sequences. Taxon 57: 109?
120.
Motley TJ, Wurdack KJ, Delprete PG. 2005. Molecular
systematics of the Catebaeeae?Chicocceae complex
(Rubiaceae): flower and fruit evolution and biogeographic
implications. American Journal of Botany 92: 316?329.
Namoff S, Luke Q, Jim?nez F, Veloz A, Lewis CE, Sosa V,
Maunder M, Fransisco-Ortega J. 2010. Phylogenetic
analysis of nucleotide sequences confirm a unique plant
intercontinental disjunction between tropical Africa, the
Caribbean, and the Hawaiian Islands. Journal of Plant
Research 123: 57?65.
Newkirk DR, Martin EE. 2009. Circulation through the
Central American Seaway during the Miocene carbonate
crash. Geology 37: 87?90.
Nixon KC, Carpenter JM. 1996. On simultaneous analysis.
Cladistics 12: 221?242.
Nylander JAA, Wilgenbusch JC, Warren DL, Swofford
DL. 2008. AWTY (are we there yet?): a system for graphical
exploration of MCMC convergence in Bayesian phylogenet-
ics. Bioinformatics 24: 581?583.
Oncken O, Hindle D, Kley J, Elger K, Victor P,
Schemmann K. 2006. Deformation of the Central Andean
Upper Plate system ? facts, fiction, and constraints for
plateau models. In: Oncken O, Chong G, Franz G, Giese P,
G?tze H-J, Ramos VA, Strecker MR, Wigger P, eds. The
Andes ? Active Subduction Orogeny. Berlin: Springer Pub-
lishing, 3?27.
Pennington RT, Dick CW. 2010. Diversification of the Ama-
zonian flora and its relation to key geological and environ-
mental events: a molecular perspective. In: Hoorn C,
Wesselingh FP, eds. Amazonia, landscape and species evo-
lution. Oxford: Blackwell Publishing, 373?385.
Pennington RT, Richardson JE, Lavin M. 2006. Insights
into the historical construction of species-rich biomes from
dated plant phylogenies, neutral ecological theory and
phylogenetic community structure. New Phytologist 172:
605?616.
Phillips O, Miller JS. 2002. Global patterns of plant diver-
sity: Alwen H. Gentry?s forest transect data set. St. Louis,
MO: Missouri Botanical Garden Press.
Pindell JL, Kennan L. 2009. Tectonic evolution of the
Gulf of Mexico, Caribbean and northern South America
in the mantle reference frame: an update. In: James KH,
Lorente MA, Pindell JL, eds. The origin and evolution
of the Caribbean plate. London: Geological Society Press,
1?55.
Pinto-S?nchez NR, Ib??ez R, Madri??n S, Sanjur OI,
Bermingham E, Crawford AJ. 2012. The Great American
Biotic Interchange in frogs: multiple and early colonization
of Central America by the South American genus Pristiman-
tis (Anura: Craugastoridae). Molecular Phylogenetics and
Evolution 62: 954?972.
Posada D. 2008. jModelTest: phylogenetic model averaging.
Molecular Biology and Evolution 25: 1253?1256.
Rabenold KN. 1990. Campylorhynchus wrens: the ecology of
delayed dispersal and cooperation in the Venezuelan
savanna. In: Stacey PB, Koenig WD, eds. Cooperative breed-
ing in birds: long-term studies of ecology and behavior.
Cambridge: Cambridge University Press, 157?196.
Read RW, Hickey LJ. 1972. A revised classification of fossil
palm and palm-like leaves. Taxon 21: 129?137.
Ree RH, Moore BR, Webb CO, Donoghue MJ. 2005.
A likelihood framework for inferring the evolution of geo-
graphic range on phylogenetic trees. Evolution 59: 2299?
2311.
Ree RH, Smith SA. 2008. Maximum likelihood inference of
geographic range evolution by dispersal, local extinction,
and cladogenesis. Systematic Biology 57: 4?14.
Richardson JF, Pennington RT, Pennington TD,
Hollingsworth PM. 2001. Rapid diversification of a
species-rich genus of Neotropical rain forest trees. Science
293: 2242?2245.
Roncal J, Blach-Overgaard A, Borchsenius F, Balslev H,
Svenning J-C. 2011. A dated phylogeny complements mac-
roecological analysis to explain the diversity patterns in
Geonoma (Arecaceae). Biotropica 43: 324?334.
Roncal J, Borchsenius F, Asmussen-Lange CB, Balslev
H. 2010. Divergence times in the tribe Geonomateae
(Arecaceae) coincide with Tertiary geological events. In:
Seberg O, Petersen G, Barford AS, Davis JL, eds. Diversity,
phylogeny and evolution in the monocotyledons. Aarhus:
Aarhus University Press, 245?265.
Roncal J, Kanh F, Millan B, Couvreur T, Pintaud J-C.
2012. Cenozoic colonization and diversification patterns
of tropical palms: evidence from Astrocaryum. Botanical
Journal of the Linnean Society. DOI: 10.1111/j.1095-
8339.2012.01265.x.
ISTHMUS OF PANAMA BIOGEOGRAPHY 299
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300
Sanmart?n I, Ronquist F. 2004. Southern hemisphere bio-
geography inferred by event-based models: plant versus
animal patterns. Systematic Biology 53: 216?243.
S?rkinen TE, Newman MF, Maas PJM, Maas H, Poulsen
AD, Harris DJ, Richardson JE, Clark A, Hollings-
worth M, Pennington RT. 2007. Recent oceanic long-
distance dispersal and divergence in the amphi-Atlantic
rain forest genus Renealmia L.f. (Zingiberaceae). Molecular
Phylogenetics and Evolution 44: 968?980.
Silver PG, Russo RM, Lithgow-Bertelloni C. 1998. Cou-
pling of South American and African Plate motion and plate
deformation. Science 279: 60?63.
Simmons MP. 2004. Independence of alignment and tree
search. Molecular Phylogenetics and Evolution 31: 874?879.
Simpson GG. 1980. Splendid isolation: the curious history of
South American mammals. New Haven, CT: Yale University
Press.
Smith BT, Klicka J. 2010. The profound influence of the
Late Pliocene Panamanian uplift on the exchange, diversi-
fication, and distribution of New World birds. Ecography 33:
333?342.
Stehli FG, Webb DS. 1985. The great American biotic inter-
change. New York: Plenum Press.
Swofford DL. 2001. PAUP* 4.0: phylogenetic analysis using
parsimony (*and other methods). Sunderland, MA: Sinauer
Associates.
Tomlinson PB. 2006. The uniqueness of palms. Botanical
Journal of the Linnean Society 151: 5?14.
Wadge G, Burke K. 1983. Neogene Caribbean plate rotation
and associated Central American tectonic evolution. Tecton-
ics 2: 633?643.
Weber R. 1978. Some aspects of the Upper Cretaeous
angiosperm flora of Coahuila, M?xico. Courier Forsc-
hungsinstitut Senckenberg 30: 38?46.
Weight LA, Crawford AJ, Rand AS, Ryan ML. 2005.
Biogeography of the t?ngara frog, Physalaemus pustulosus:
a molecular perspective. Molecular Ecology 14: 3857?
3876.
Weir JT, Bermingham E, Schluter D. 2009. The Great
American Biotic Interchange in birds. Proceedings of the
National Academy of Sciences, USA 106: 21 737?21 742.
Whitmore FC Jr, Stewart RH. 1965. Miocene mammals
and Central American Seaways: fauna of the Central Zone
indicates separation of Central and South America during
most of the Tertiary. Science 148: 180?185.
Wilgenbusch JC, Warren DL, Swofford DL. 2004. AWTY:
a system for graphical exploration of MCMC convergence
in Bayesian phylogenetic inference. Available at: http://
ceb.csit.fsu.edu/awty (accessed 17 January 2012)
Wing SL, Herrera F, Jaramillo CA, G?mez-Navarro C,
Wilf P, Labandeira CC. 2009. Late Paleocene fossils from
the Cerrej?n formation, Colombia, are the earliest record of
Neotropical forest. Proceedings of the National Academy of
Sciences, USA 106: 18 627?18 632.
Yang Z. 2006. Computational molecular evolution. Oxford:
Oxford University Press.
Yu Y, Harris AJ, He X. 2010. S-DIVA (statistical dispersal-
vicariance analysis): a tool for inferring biogeographic
histories. Molecular Phylogenetics and Evolution 56: 848?
850.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Figure S1. Chronogram from BEAST analysis with all posterior probability (PP) support values shown for
nodes under PP = 1.0.
300 C. D. BACON ET AL.
? 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 287?300