Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev
Short Communication
Phylogeny of the island archipelago frog genus Sanguirana: Another
endemic Philippine radiation that diversified ‘Out-of-Palawan’ q
Rafe M. Brown a,⇑, Yong-Chao Su a, Brenna Barger a, Cameron D. Siler b, Marites B. Sanguila c,
Arvin C. Diesmos d, David C. Blackburn e
a
Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045-7561, USA
Sam Noble Oklahoma Museum of Natural History and Department of Biology, University of Oklahoma, Norman, OK 73072-7029, USA
Arts and Sciences Program, Saturnino Urios University, San Francisco St., 8600 Butuan City, Philippines
d
Herpetology Section, Zoology Division, Philippine National Museum, Burgos St., Ermita 1000, Manila, Philippines
e
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
b
c
a r t i c l e
i n f o
Article history:
Received 16 July 2015
Revised 9 October 2015
Accepted 10 October 2015
Available online xxxx
Keywords:
Cascade frogs
Geographic radiation
Palawan Arc Hypothesis
Pleistocene Aggregate Island Complexes
(PAICs)
Stream frogs
a b s t r a c t
Recent higher-level frog phylogenetic analyses have included a few members of the endemic Philippine
frog genus Sanguirana. Although the monophyly of the group has never been disputed, the recent
phylogenetically-supported inclusion of the Palawan Wood Frog (Sanguirana sanguinea) in this clade
was highly unexpected. In addition, species boundaries and relationships remain unclear and new species
continue to be discovered. We estimate the phylogeny for this endemic Philippine genus using two
mitochondrial gene regions and six nuclear loci and complete sampling for all known species. We use
a time-calibrated Bayesian estimate of phylogeny and model-testing approach to biogeographic inference
to infer ancestral areas and probable means of diversification. These analyses identify Sanguirana as an
additional clade for which the biogeographic ‘Out-of-Palawan’ biogeographic scenario is unambiguously
preferred. This study lends additional support to recent work suggesting that a substantial portion of
Philippine vertebrate megadiversity originated via colonization of the archipelago from the Palawan
microcontinent, with subsequent invasion of oceanic islands (e.g., range expansion over Huxley’s
Modification of Wallace’s Line), numerous instances of overwater dispersal, and geographic radiation
across the archipelago.
Ó 2015 Elsevier Inc. All rights reserved.
1. Introduction
Our limited understanding of the biogeographic patterns and
evolutionary processes behind Southeast Asia’s exceptionally high
levels of vertebrate diversity is both a crippling limitation for conservation biologists (Woodruff, 2010) and a remarkable opportunity for evolutionary biologists and biogeographers (Brown and
Diesmos, 2009; Lohman et al., 2011; Brown et al., 2013). Studies
Southeast Asian biodiversity have been hampered by the patchy
and non-comprehensive nature of basic survey work in its forests
(Lim et al., 2008), the deterioration, lack of financial support, and
threats to existing biodiversity collections (Kemp, 2015), the
q
This paper was edited by the Associate Editor A. Larson.
⇑ Corresponding author at: Biodiversity Institute, 1345 Jayhawk Blvd., Lawrence,
KS 66045, USA. Fax: +1 785 864 5335.
E-mail addresses: [email protected] (R.M. Brown), [email protected] (Y.-C. Su),
[email protected] (B. Barger), [email protected] (C.D. Siler), mbsanguila@
urios.edu.ph (M.B. Sanguila), [email protected] (A.C. Diesmos),
[email protected] (D.C. Blackburn).
lugubrious pace of taxonomic work (Joppa et al., 2011), and
country-specific, idiosyncratic, and variable policies of natural
resource management (La Viña et al., 1997; Lim et al., 2008;
Meijaard, 2011).
Home to numerous celebrated clades of co-distributed
terrestrial vertebrates (Brown and Diesmos, 2009), the Philippine
Archipelago recently has been the focus of several integrative studies of amphibian radiations (Setiadi et al., 2011; Blackburn et al.,
2013; Brown and Siler, 2013; Brown et al., 2013, 2015). One moderately sized clade is the endemic frog genus Sanguirana (formerly
the Rana everetti Complex; Brown et al., 2000), which consists of
seven described and morphologically diagnosable species and
one or two undescribed ‘‘cryptic” species (Brown et al., 2000;
Fuiten et al., 2011). Additional new species most likely await discovery in unsurveyed portions of the archipelago (Brown et al.,
2013; Brown, 2015).
In a recent review, Brown et al. (2013) distinguished between
the archipelago’s partially or fully characterized adaptive
radiations (e.g., Blackburn et al., 2013; Brown et al., 2015) and
http://dx.doi.org/10.1016/j.ympev.2015.10.010
1055-7903/Ó 2015 Elsevier Inc. All rights reserved.
Please cite this article in press as: Brown, R.M., et al. Phylogeny of the island archipelago frog genus Sanguirana: Another endemic Philippine radiation that
diversified ‘Out-of-Palawan’. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.010
2
R.M. Brown et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
the possibly non-adaptive, ‘‘geographic” radiations (e.g., Setiadi
et al., 2011; Brown and Siler, 2013). The latter, loosely defined category (Brown et al., 2013) includes clades with one or more representative species on each island bank, or Pleistocene Aggregate
Island Complex (PAIC; Brown and Diesmos, 2009; Fig. 1). In these
clades, species have been characterized as ecologically similar with
little to no evidence of a phenotype-environment correlation or
within-island, ecologically associated diversification (Brown
et al., 2000, 2013; Brown and Siler, 2013). Of particular interest
are clades that show a mixture of diversification patterns, with single ecological generalist species on some islands, but evidence of
intra-island diversification, habitat specialization, and multiple
sympatric species on other islands (Setiadi et al., 2011; Brown
et al., 2013, 2015).
We estimate the phylogeny and biogeographic history of one
such group: Philippine endemic stream frogs of the genus
Sanguirana (Brown et al., 2000; Fuiten et al., 2011). Aside from
being one of only two amphibian genera endemic to the country
(the other being Platymantis; Brown et al., 2015), Sanguirana is
interesting because of its pattern of species’ distributions. The
genus consists of at least eight species (Fuiten et al., 2011), with
all taxa restricted to individual PAICs (Brown et al., 2000). Several
of the species (S. albotuberculata, S. everetti, S. sanguinea, and S. sp.
[undescribed]) possess exclusive, non-overlapping distributions
isolated to single PAICs or island subsets within PAICs, but the
remainder (S. aurantipunctata, S. igorota, S. luzonensis, and
S. tipanan) features some degree of sympatry in the mountains of
Luzon Island (Figs. 1 and 2; Brown et al., 2000).
Here we infer the biogeographic history of this group and ask
whether any of the previously hypothesized, shared mechanisms
of diversification for Philippine terrestrial vertebrates (Brown
et al., 2013) apply to Sanguirana. Our multilocus phylogenetic estimate and ancestral inference of biogeography identifies the genus
as yet another clade with a biogeographic history consistent with
the ‘Out-of-Palawan’ biogeographic scenario (Blackburn et al.,
2010; Esselstyn et al., 2010; Siler et al., 2012; Brown et al.,
2013). As such, the genus Sanguirana represents the first amphibian clade for which the Palawan Arc Hypothesis (Blackburn et al.,
2010; Siler et al., 2012) is a tractable explanation for the initial isolation, biogeographic origin, and subsequent diversification of one
of the archipelago’s more spectacular and completely endemic
radiations (Brown and Diesmos, 2009; Brown et al., 2013).
2. Materials and methods
2.1. Taxon sampling and data collection
Ingroup sampling included 161 individuals collected from 47
localities, including all known species of Sanguirana (Fig. 1;
Appendix A, Supplemental Material). We selected closely related
outgroup species Glandirana minima and Hylarana erythraea, on
Fig. 1. Map of the Philippine archipelago (A) with sampling color coded by species (see key). Lighter blue shadings indicate shallow seas and the underwater bathymetric
contour forming the major Pleistocene Aggregate Island Complexes (PAICs; Brown and Diesmos, 2009). Hypothesized relationships of Sanguirana species (B), depicted by the
consensus tree resulting from the post-burnin posterior distribution from the Bayesian analysis of the concatenated dataset. Strongly supported nodes (P0.95 Bayesian PP;
P70% ML) are denoted with black dots) and moderately supported nodes (0.90–0.95 Bayesian PP) are indicated with gray dots. Bayesian analysis of nuclear genes only (C)
resulted in weakly-supported differences in branching order among species but resolve the paraphyly of S. luzonensis (with respect to S. igorota and S. tipanan); (D) deep
coalescence as one possible explanation for incongruence between mtDNA and nDNA gene lineages. (For interpretation of the references to color in this figure legend, the
reader is referred to the web version of this article.)
Please cite this article in press as: Brown, R.M., et al. Phylogeny of the island archipelago frog genus Sanguirana: Another endemic Philippine radiation that
diversified ‘Out-of-Palawan’. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.010
R.M. Brown et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
3
Fig. 2. Time-calibrated Bayesian topology from BEAST (see text for results from individual calibration schemes) with approximate geological reconstructions from Hall (1998)
and the results of ancestral range estimation under the best-fit, 3-parameter DIVALIKE+J model of geographical range evolution (Table 2) implemented in the R package
BioGeoBEARS (Matzke, 2013). Color-coded boxes on nodes correspond to PAIC ancestral range estimates, indicated on right (colored vertical bars). (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of this article.)
the basis of uncontroversial higher-level phylogenetic relationships of the family Ranidae (Wiens et al., 2009), and sequenced a
total of 6098 nucleotides from two mitochondrial gene regions
and six nuclear loci (Table 1). Primers, PCR methods, thermal profiles, and sequencing protocols follow our recent phylogenetic
studies (Brown and Siler, 2013; Brown et al., 2015). We visualized
products on 1.5% agarose gels and used ABI BigDye Terminator v3.1
sequencing chemistry (Life Technologies, Grand Island, NY) for
cycle sequencing. PCR products and sequencing reactions were
purified using ExoSAP-IT and Sephadex cleanups, respectively
(Amersham Biosciences, Piscataway, NJ). Purified products were
analyzed with an ABI Prism 3730xl Genetic Analyzer, and
sequences were assembled and edited using Geneious vR8.1.7
(Kearse et al., 2012). All novel sequences were deposited in
GenBank (Appendix A, Supplemental Material).
2.2. Sequence characteristics, alignment, and phylogenetic analyses
Initial alignments were produced in MAFFT v7.221 (Katoh and
Standley, 2013) with slight manual adjustments. To assess gene
congruence, we estimated gene trees with Bayesian and likelihood
analyses and compared estimates from these independent partitions for the presence of strongly supported conflict between gene
regions. Finding none, we concatenated data for subsequent analyses. We then assembled two datasets: one with all genes included
(but with missing nuclear data for many individuals [Table 1];
Appendix A, Supplemental Material) and another reduced to samples with near-complete nuclear gene sampling. Because exploratory comparative analyses yielded the same strongly supported
nodes, we felt justified in including all available data in subsequent
phylogenetic analyses.
Partitioned Bayesian analyses were conducted in MrBayes v3.2.5
(Ronquist and Huelsenbeck, 2003). We partitioned the ribosomal
RNA mitochondrial sequences by region (12S, tRNAval, and 16S),
nuclear DNA was partitioned by locus, with gene-specific proteincoding regions partitioned by codon position (Table 1). The Akaike
Information Criterion (AIC), as implemented in jModelTest v2.1.7
(Darriba et al., 2012, was used to select the best model of nucleotide
substitution for each partition (Table 1). We ran four MCMC analyses, each with four Metropolis-coupled chains, an incremental heating of 0.02, and an exponential distribution with 25 as the rate
parameter prior on branch lengths. All analyses were run for
Please cite this article in press as: Brown, R.M., et al. Phylogeny of the island archipelago frog genus Sanguirana: Another endemic Philippine radiation that
diversified ‘Out-of-Palawan’. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.010
4
R.M. Brown et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Table 1
Loci, number of sequences (N), characteristics, partitioning, and results of model selection procedure.
Locus
N
Total characters
Pars-inform char’s
Un-informative char’s
Variable char’s
Mean p-distance
Substitution model
12S
tRNA-Val
16S
CLT-1st
CLT-2nd
CLT-3rd
CPT-1st
CPT-2nd
CPT-3rd
CXCR-1st
CXCR-2nd
CXCR-3rd
RAG1-1st
RAG1-2nd
RAG1-3rd
Tyro-1st
Tyro-2nd
Tyro-3rd
DNAH3-1st
DNAH3-2nd
DNAH3-3rd
161
154
151
28
28
28
21
21
21
43
43
43
23
23
23
40
40
40
26
26
26
485
70
1457
228
228
227
249
249
248
197
197
196
202
203
202
181
181
181
306
306
306
129
25
428
12
8
28
1
3
14
4
1
23
3
11
7
5
21
4
5
2
16
67
8
258
7
3
10
8
7
23
1
0
7
1
23
6
8
31
13
5
4
9
196
33
686
19
11
38
9
10
37
5
1
30
4
34
13
13
52
17
10
6
25
1.32972
0.97069
1.83154
0.13111
0.06915
0.31727
0.03614
0.04217
0.18975
0.04158
0.01204
0.34387
0.08108
0.2354
0.13289
0.09734
0.4392
0.18681
0.03268
0.01961
0.09818
TrN+C
K80+C
GTR+I+C
TPM1uf+I
TrN+I
TPM1uf+I+C
HKY
HKY
K80+I
JC
TrN
TPM1uf+I+C
F81
HKY+C
HKY+I
TPM1uf+C
HKY+C
HKY
F81
HKY
HKY
20 107 generations, with parameters and topologies sampled
every 1000 generations. We assessed stationarity with Tracer v1.6
(Rambaut and Drummond, 2007) and convergence with AWTY
(Wilgenbusch et al., 2004). Stationarity was achieved after 5 106
generations (first 25% samples), which we discarded as burn-in.
Partitioned maximum likelihood (ML) analyses were conducted
in RAxMLHPC v8.0.0 (Stamatakis, 2014) on the concatenated dataset using the same partitions (Table 1) but with the GTR+ C model
for each. One hundred replicate inferences were performed, each
initiated with a random starting tree. Nodal support was assessed
with 1000 bootstrap pseudoreplicates. Alignments and resulting
topologies were deposited in Dryad (doi: 10.5061/dryad.6394c).
2.3. Divergence time estimation and biogeographic inference
We used BEAST v1.8.2 (Drummond et al., 2012) to estimate
divergence times. We unlinked clock models and original substitution rates per gene/partition, and employed the following priors for
two calibration strategies: (1) we applied a range of empirically
observed amphibian divergence rates (1.4% Mya 1, 95%
HPD = 0.8–1.9%) following Sanguila et al. (2011) as the rate calibration for the mitochondrial genes in our data set; (2) for comparison, we applied the time estimate of the approach of the oceanic
Philippines to the Palawan microcontinent block (8 Mya, 95%
HPD = 10–6; Hall, 1998) to provide a crude estimate of the origin
of the oceanic Philippine lineage. We then combined four separate
runs for each calibration (25% burn-in for each) and considered
effective sample sizes adequate if >200. We diagnosed convergence
with Tracer v1.6 and used TreeAnnotator v1.8.2 to generate our
final maximum clade credibility topology.
We used BioGeoBEARS (Matzke, 2013) to gain insight into
potential speciation modes and to estimate ancestral geographical
ranges. We considered a total of six models (Matzke, 2013): Disper
sal-Extinction-Cladogenesis (DEC; Ree and Smith, 2008), Ronquist’s
(1997) Dispersal-Vicariance Analysis (DIVA; Ronquist, 1997), and
the BayArea model (Landis et al., 2013); and an additional parameter j that was considered for each model to evaluate founder-event
speciation, which could be associated with long distance dispersal
and subsequent divergence of colonizing lineages (Matzke, 2013).
We then estimated biogeographic ancestral ranges and transitions
thereof under the best-fit model (selected with AIC).
3. Results
3.1. Phylogeny
Bayesian and likelihood analyses (Figs. 1 and 2) of the complete
dataset strongly support a monophyletic Philippine Sanguirana
(MrBayes posterior probabilities [PP] = 1.00, Maximum Likelihood
bootstrap support [MLBS] = 100). Sanguirana sanguinea from
Palawan Island is the sister taxon to the remaining clade of oceanic
Philippine lineages (PP = 0.99, MLBS = 80; Fig. 1). Within this clade
of oceanic Philippine species are three strongly supported taxa
whose relationships to each other are not resolved with strong support: (1) the Luzon endemic S. aurantipunctata, (2) the Mindanao
clade of S. albotuberculata + S. everetti (PP = 1.00, MLBS = 100), and
(3) a clade in which an undescribed species from the West Visayan
islands (Figs. 1 and 2; PP = 0.99, MLBS = 93) is sister to a clade of species from Luzon (S. igorota, S. luzonensis, and S. tipanan; PP = 0.73,
MLBS = 88). The relationships among S. igorota, S. luzonensis, and
S. tipanan remain poorly resolved (Fig. 1). Weakly supported differences between the mitochondrial gene tree (not shown; identical to
the concatenated tree in Fig. 1B) and a separate nuclear topology
(Fig. 1C), involves a possibly non-monophyletic S. luzonensis with
respect to S. igorota and S. tipanan (Fig. 1).
3.2. Biogeographic inference and time frame for diversification
We subsampled 49 individuals (at least two samples/clade from
the 161-individual dataset) with near-complete mitochondrial and
nuclear sequences to estimate the divergence times among the
major clades. When our amphibian mitochondrial molecular clock
(1.4% divergence between species Mya 1) was applied, we
estimated the oldest ingroup node as 12.1 Mya (95% HPD = 16.9–
7.7), which approximates the divergence (14.1 Mya, 95%
HPD = 18.3–10.2) inferred when using our geological calibration
(10–6 Mya, Hall, 1998). The estimated divergence times for the
oceanic clade were nearly identical (molecular clock: 7.8 Mya,
95% HPD = 10.6–5.2; geology: 7.9 Mya, 95% HPD = 9.5–6.4).
Divergence times within the oceanic Philippines were similarly
coincident, and dated during the late Miocene to Pliocene (Fig. 2).
The best-fit biogeographic model selected by AIC weights was
Matzke’s (2013) likelihood implementation of the DIVA model
(i.e., two-parameter model; dispersal allowed but penalized
Please cite this article in press as: Brown, R.M., et al. Phylogeny of the island archipelago frog genus Sanguirana: Another endemic Philippine radiation that
diversified ‘Out-of-Palawan’. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.010
5
R.M. Brown et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Table 2
Results of biogeographic model selection procedure via Akaike Information Criterion assessment of model fit (Matzke, 2013).
Model
DIVALIKE+J
DEC
DEC+J
DIVALIKE
BAYAREALIKE+J
BAYAREALIKE
LnL
8.098662
9.534161
8.927847
11.064518
10.410781
16.305238
Numparams
d
3
2
3
2
3
2
1.00E
1.00E
1.00E
7.87E
1.00E
9.80E
e
12
12
12
03
07
03
relative to vicariance; Ronquist, 1997), which incorporates dispersal to a geographic area not observed in the parental lineages
(DIVALIKE+J; Table 2). The ancestral range estimate based on this
model inferred a process of vicariance for diversification between
the ephemerally accreted (or, at least, adjacent) Palawan microcontinent + proto-Luzon block (Hall, 1998; Brown and Diesmos,
2009), which then separated as the latter slipped farther north
along the Philippine trench (Fig. 2; Hall, 1998; Brown et al.,
2013). Subsequently, because the oceanic Philippines arrived at
its current configuration within the last eight million years (Hall,
1998; Brown and Diesmos, 2009), we infer that speciation during
this period was associated with repeated bouts of overwater
dispersal and colonization between isolated PAICs (Luzon to
Mindanao 7.3 Mya; Luzon to Western Visayas 5.9 Mya; Fig. 2).
4. Discussion
4.1. Phylogeny
Our phylogenetic estimate identifies weakly supported differences between mitochondrial and nuclear dataset partitions. These
discrepancies involve the first-branching lineages within the
apparently
rapidly-radiating
oceanic
Philippines
clade
(Fig. 1B and C), and also the non-monophyly of S. luzonensis with
respect to S. igorota and S. tipanan (Fig. 1D). The latter conceivably
could be explained by the presence of a cryptic species (Sierra
Madre and Zambales mountains ranges of Luzon and possibly
Marinduque Island; Fig. 1B), maintenance of ancestral polymorphism, deep coalescence of mitochondrial gene lineages, and/or
the stochastic nature of lineage sorting in the coalescent
(Fig. 1D). Distinguishing between these hypotheses is beyond the
scope of the current dataset given the lack of support at some
nodes and limited number of loci available.
4.2. ‘Out-of-Palawan’ biogeography in Philippine stream frogs
The analysis presented here identifies another Philippine radiation for which the Palawan Ark Hypothesis (Blackburn et al., 2010;
Siler et al., 2012; Brown et al., 2013) best fits the available data.
Because of low support for the clade ((S. everetti + S. albotuberculata) (S. sp. Negros-Panay (S. luzonensis (S. igorota + S. tipanan + S.
luzonensis))))), we are unable to infer the sequence of island colonization following the initial invasion of the oceanic portions of
the archipelago from Palawan (Fig. 1D). We expect that an
improved, fine-scale biogeographic inference may be possible with
information from additional loci. Despite the lack of support for the
sequence of island colonization (and order of first branching within
the oceanic Philippine clade; Fig. 1B and C), the genus Sanguirana
clearly diversified within the Philippines after an initial invasion
from the Palawan microcontinent. It has not escaped our attention
that if current phylogenetic estimates are correct, and Glandirana is
in fact Sanguirana’s closest mainland relative (Wiens et al., 2009),
then biogeography of Sanguirana is similar to other
‘Out-of-Palawan’ taxa in that its closest relatives apparently are
not present on landmasses of the Sunda Shelf, but instead are more
1.00E
1.00E
2.36E
1.00E
1.00E
1.05E
12
12
09
12
07
01
j
AIC
Delta-AIC
AIC Wt.
0.05097011
0
0.04630856
0
0.07690819
0
22.197324
23.068322
23.855694
26.129036
26.821562
36.610476
0.870998
0
0.787372
3.060714
3.75324
13.542154
0.58
0.37
0.25
0.08
0.06
0.00
diverse and widespread on the Asian mainland (Blackburn et al.,
2010; Siler et al., 2012; Brown et al., 2013).
4.3. Common mechanisms of diversification for land vertebrates of
Southeast Asian island archipelagos?
Much attention has been paid to hypotheses of common mechanisms of diversification in terrestrial vertebrates of the Philippines,
an iconic Southeast Asian island archipelago (Woodruff, 2010;
Lohman et al., 2011; Brown et al., 2013). In the Philippines, a
disproportionate amount of this attention has focused on the
‘PAIC-paradigm,’ its impact in unrelated taxa, deviations from the
model, and other recent (Pleistocene) explanations (reviews:
Brown and Diesmos, 2009; Brown et al., 2013; Oaks et al., 2013).
However, more recent inferences from increasingly robust multilocus molecular phylogenies (Esselstyn et al., 2010; Setiadi et al.,
2011; Brown et al., 2015) suggest that alternate explanations are
plausible, and clearly have contributed to establishing Philippine
vertebrate megadiversity (Brown and Diesmos, 2009). These include
within-island habitat connectivity/discontinuity, ecological divergence along altitudinal gradients, contingency in processes of insular community assembly, and the possibility paleo-transport of
ancient isolated lineages on continental land fragments during the
assembly of the archipelago (Hall, 1998; Blackburn et al., 2010;
Brown et al., 2013). The Palawan Ark Hypothesis is one such explanation that may characterize the evolutionary history of more terrestrial biodiversity in the oceanic Philippines than has generally
been appreciated (Esselstyn et al., 2010). Moving beyond the PAIC
paradigm toward the acceptance of a plurality of shared mechanisms and a greater appreciation of overseas dispersal has been an
inevitable and welcomed consequence of the accumulation new
data from recent biodiversity surveys throughout the archipelago
(Brown et al., 2013).
Acknowledgments
We thank the Biodiversity Monitoring Bureau (BMB) of the
Philippine government for facilitating permits, M. Diesmos and A.
C. Alcala for collaboration and logistical support, and the U.S.
National Science Foundation (DEB 073199, 0334952, 0743491,
0804115, and 1418895) for supporting our research.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.ympev.2015.10.
010.
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Please cite this article in press as: Brown, R.M., et al. Phylogeny of the island archipelago frog genus Sanguirana: Another endemic Philippine radiation that
diversified ‘Out-of-Palawan’. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.010