The Eurasian invasion: phylogenomic data reveal multiple Southeast Asian origins for Indian Dragon Lizards
© Grismer et al. 2016
Received: 17 December 2015
Accepted: 8 February 2016
Published: 19 February 2016
The Indian Tectonic Plate split from Gondwanaland approximately 120 MYA and set the Indian subcontinent on a ~ 100 million year collision course with Eurasia. Many phylogenetic studies have demonstrated the Indian subcontinent brought with it an array of endemic faunas that evolved in situ during its journey, suggesting this isolated subcontinent served as a source of biodiversity subsequent to its collision with Eurasia. However, recent molecular studies suggest that Eurasia may have served as the faunal source for some of India’s biodiversity, colonizing the subcontinent through land bridges between India and Eurasia during the early to middle Eocene (~35–40 MYA). In this study we investigate whether the Draconinae subfamily of the lizard family Agamidae is of Eurasian or Indian origin, using a multi locus Sanger dataset and a novel dataset of 4536 ultraconserved nuclear element loci.
Results from our phylogenetic and biogeographic analyses revealed support for two independent colonizations of India from Eurasian ancestors during the early to late Eocene prior to the subcontinent’s hard collision with Eurasia.
These results are consistent with other faunal groups and new geologic models that suggest ephemeral Eocene land bridges may have allowed for dispersal and exchange of floras and faunas between India and Eurasia during the Eocene.
KeywordsAgamidae Draconinae Eocene Eurasia India Faunal exchanges Landbridges
The collision of the Indian subcontinent (ISC) into Eurasia caused the formation of some of the world’s most iconic deserts and mountain ranges, dramatically changing Asian climates, while simultaneously sculpting its biodiversity. Much interest has centered on investigating the evolutionary and geological processes that have influenced the origins and diversification of the ISC’s unique biotas (; and references therein). Phylogenetic studies of birds, dipterocarp trees, terrestrial gastropods, crabs, freshwater fish, and certain groups of amphibians, suggests these lineages originated on the ISC and were a source of biodiversity for regions of Asia and areas as far west as Africa after the Indian Plate split off from Gondwanaland [2–7]. However, a suite of phylogenetic studies across a variety of other taxa suggest an alternative biogeographic hypothesis postulating Eurasia as the ancestral source of diversity for the ISC. In these groups Asian lineages dispersed to, and successfully colonized, the subcontinent before its hard collision with Eurasia 25–30 MYA [8–12].
The previous lack of geologic models describing the fine scale events of the final 50 million years of the ISC’s collision, left researchers with no mechanistic explanation for the striking differences between these two “ISC faunal origin” hypotheses. Fortunately, newer models are available that take into account continental connections between the approaching ISC and areas of mainland Asia prior to the ISC’s collision with Eurasia [13–15]. Acton  and Ali and Aitchison  hypothesized that between 34–55 MYA (middle Eocene-late Eocene), India was connected to Eurasia via land-bridges with Sumatra, and then along what is now the Thai-Malay Peninsula and Burma (which would have been one land mass during this time). Two recent studies have recovered phylogenetic support for these Eocene land bridges and hypothesized that these pre-collision continental connections would have allowed for faunal exchanges between the ISC and Eurasia as the ISC continued northward [7, 16]. We present data from a diverse radiation of Indian and Southeast Asian lizards that provide an additional model system, with largershould be large not "larger" amounts of generic diversity of Indian lineages and Asian lineages, to test for phylogenetic support for these Eocene land bridges, which we refer to as the Eocene Exchange Hypothesis (EEH).
Since Moody  and Macey et al. , new Draconinae genera have been discovered, and previously unsampled rare genera have been collected, providing additional genetic material for reanalysis of draconine relationships. The lower per-base cost of next-generation sequencing has also led to the development of genomic methods extending the number of genetic markers that have limited the phylogenetic resolution in previous studies. Here, we generate a genomic data set of 4536 nuclear loci derived from ultraconserved elements (UCEs), along with traditional Sanger sequencing data, to resolve the problematic relationships within the Draconinae reported by Macey et al. . With the addition of new taxa, and genomic sequence-capture data, analyzed in combination with newly developed geological models, we are poised to reinterpret the biogeographic origins of Indian and Southeast Asian draconine lineages. Specifically, we tested (1) Moody’s  pre-collision hypothesis versus Macey et al.  post-collision hypothesis for the origins of Indian lineages; and (2) suggest that a conclusion in favor of Moody’s  pre-collision hypothesis would show phylogenetic support for the Eocene land bridge connections proposed by Acton  and Atchison et al. . We term this the Eocene Exchange Hypothesis (EEH).
DNA extraction, Sanger mitochondrial and nuclear DNA sequence data collection
Genomic DNA was extracted from muscle or liver tissue samples on loan form La Sierra University, Villanova University, the California Academy of Sciences, the Zoologisches Forschungsmuseum Alexander Koenig, and the Chicago Field Museum. Extractions were preformed using a DNeasy tissue kit (Qiagen, Inc.) and sequenced for the mitochondrial and nuclear genes, ND2 (primers from ) and RAG-1 (primers from ), respectively, using standard PCR and Sanger sequencing protocols. We edited the sequences and aligned them within Geneious Pro 5.0.4 (http://www.geneious.com, ) and these new sequence data were combined with existing data from  and  (Additional file 1: Table S1). In total, the dataset included 17 of the 26 draconine genera, including all but two of the Indian genera (Psammophilus and Coryphophylax). Hyrdosaurus and Physignathus were not included as their phylogenetic affinities are with other agamid lineages outside of the Draconinae . At least three species (or individuals if the genus was monotypic) per genus were sampled, for a total of 44 individuals. ND2 and RAG-1 were selected as they are the most frequently sequenced markers across acrodont lizards and therefore provide maximum taxonomic coverage. We used these markers to preliminarily place new genera in a phylogenetic context, and as a guide tree in our selection of genera for UCE development to resolve problematic relationships. No experimental research was carried out on these animals in this study.
Ultraconserved elements (UCE) data collection
Phylogenetic and biogeographic analyses
We first used Bayesian analyses with MrBayes 3.2.2  of the ND2 and RAG-1 datasets independently in the context of the entire Agamidae to ensure that Draconinae was monophyletic. Once monophyly and lack of conflict between loci was established, we concatenated the two gene partitions for subsequent analyses. We used uniform priors in MrBayes 3.2.2 and partitioned the dataset by locus and codon within each locus for just the members Draconinae sub-family. We then assigned the GTR+ Γ substitution model for each partition and used three chains (two hot and one cold), and carried out 100 million generations, sampled every 10,000 generations. Due to the risk of substitution saturation, we performed analyses including and excluding the third codon position for the ND2 alignment. Convergence between chains, likelihood scores, and estimate sample size (ESS) values were evaluated using Tracer 1.6  In order to obtain a reliable root age for divergence-time estimates within Draconinae, we expanded our ND2 and RAG-1 datasets to include data from all acrodont lineages. We analyzed this expanded dataset using eight acrodont fossils (Additional file 2: Table S2) within a Bayesian framework in BEAST 2.3  using the fossilized-birth-death model [35, 36]. The fossilized-birth-death process provides a model for the distribution of speciation times, tree topology, and distribution of lineages sampled before the present, and treats the fossil observations as part of the prior on node time estimates. We used the root age for the Draconinae resulting from this analysis (85 MYA) as a minimum-age calibration for the root of the Draconinae for subsequent time of divergence estimates within the Draconinae clade.
We performed likelihood analyses in RAxML v.8.1.20  on concatenated datasets for the incomplete (4536 loci) and complete (1114 loci) matrices, using the GTR+ Γ substitution model, and ran 100 fast bootstrap replicates. In addition to the concatenated analysis, maximum likelihood gene trees were constructed for each of the UCE loci included in the complete matrix using Phyluce with RAxML v.8.1.20 , under default settings. Phyluce and RAxML were also used to generate gene trees for 500 multi-locus bootstraps . Custom R-scripts (R v3.2.0; R Core Team 2015) and the R library Phybase  were then used to infer the STEAC  summary species tree for the original and bootstrapped data.
Grafted phylogeny and divergence dating
Using 85 MYA as a minimum age limit for the ancestor of the Draconinae, divergence dates for subclades were estimated in BEAST 2.3 using the ND2 and RAG-1 datasets with linked clock and tree models. We applied Birth-Death tree priors and constrained the relationships to match the results from the analyses of the UCE loci (blue nodes: Fig. 2b) and let the relationships within each species group be estimated by the BEAST analyses. We used a relaxed uncorrelated lognormal clock model and an exponential prior for the mean rate of each partition. Default values were used for all other priors, and the analysis was run for 150 million generations sampling every 12,000 generations, with chain stationarity, and ESS values were evaluated in Tracer 1.6. The first 25 % of trees were discarded as burn-in and the maximum clade credibility tree with median node heights was summarized using TreeAnnotator 2.3 . We converted our alignments to fasta format using seqmagick (http://seqmagick.readthedocs.org/en/latest/). Then, with the estimate for divergence between Mantheyus and other draconine species of 85MYA, we estimated the TMRCA of subclades based on pairwise Hamming distances  between UCE loci (with a sequence saturation correction of 0.95) calculated through fastphylo , assuming a naïve strict clock. We carried out the calculations using a custom R-script . Any loci where subgroup divergence times exceeded those of the calibration time were discarded due to the likelihood of incomplete lineage sorting and/or excessive rate variation. Using the same methods, we then estimated the time to most recent common ancestor (TMRCA) of the Draco + Ptyctolaemus and species group 1–4 clades using the estimated age of the Non-Mantheyus clade. The estimate of the TMRCA of species group 1–4 was then used to age the split between Acanthosaura and Pseudocalates (species group 1), and the ancestor of species groups 2/3/4. The species group 2/3/4 TMRCA estimate was then used to age the split between Salea and Calotes (species group 2 and 3), and the ancestor of species group 4. Finally, the estimate for the TMRCA of species group 4 was used to obtain an estimate of the TMRCA of Certaophora/Lyriocephalus/Cophotis.
Ancestral area reconstructions were performed using likelihood and Bayesian methods in LAGRANGE within the program RASP 3.0 , and in RevBayes 10.10  respectively. Taxa were assigned to their biogeographic zone (Fig. 1) based on their modern day distributions and RevBayes reconstructions were visualized using the online resource Phylowood . Traditionally, the Philippines is not classified as part of Sundaland however, we included taxa from this archipelago in the Sundaland biogeographic area because the entire Philippine agamid fauna is Sundaic in origin.
Sanger mitochondrial and nuclear data phylogenetic analyses
The Bayesian analyses of the combined Sanger dataset recovered new relationships that have not been reported in any previous study (Fig. 2a). Mantheyus was recovered as sister to the remaining Draconinae. The next lineage to diverge was a well-supported clade containing Draco, and Ptyctolaemus (Fig. 2a). Lastly, there were four well-supported species groups (brown nodes: Fig. 2a). The relationships within each of these species groups were well supported. However, the relationships between the species groups were poorly resolved and characterized by short branches (pink nodes: Fig. 2a). As the resolution of the relationships between the species groups is vital for testing hypotheses of Indian or Eurasian origins, representatives of the taxa from each of these species groups were included in a phylogenetic reconstruction from analyses of UCE data.
Sequence-capture data phylogenetic analyses
There were 4536 loci with data for at least 75 % of the n = 23 individuals included in this study. These loci had an average length of 644.7 bp (S.D. = 249.7 bp), of which an average of 10.5 % of sites (S.D. = 20.0 %) were parsimony informative. The average amount of missing data per locus was 23.6 % (S.D. = 19.4 %), including both missing individuals (up to 25 % of individuals at each locus) and shorter sequence lengths for individuals that were present (Additional file 3: Table. S3). All analyses of the sequence-capture data were successful in resolving the problematic relationships recovered from the Sanger data (blue nodes; Fig. 2b) and recovered each of the four species groups within the Draconinae, with high support (brown nodes; Fig. 2b), consistent with the results from the Sanger datasets.
Biogeographic analyses, divergence dating, and ancestral areas
In this study, we utilized unprecedented sampling of the Draconinae, both in taxonomic diversity and genetic markers, to give fresh biogeographic insight into the origins of the Indian and Southeast Asian Draconinae lineages. In particular, the thousands of loci generated using sequence-capture and next-generation sequencing were successful in resolving previously problematic relationships within the Draconinae (brown nodes: Fig. 2). Using the fully resolved UCE phylogeny to constrain the topology of our Sanger dataset, we generated a grafted Bayesian time tree (Fig. 3a), which supported the hypothesis that there were at least two independent colonization events of India by Southeast Asian lineages during the Eocene. These results favor Moody’s  pre-collision hypothesis with the estimated times of the Eurasian invasions in accordance with the Eocene land bridges proposed by Acton,  and Ali and Aitchison . These hypothesized land bridges would have connected areas of Eurasia (now Sundaland and the Thai-Malay peninsula) and the ISC before its collision, and are the likely conduits for terrestrial faunal exchange and range expansion in the lineages leading to today’s Indian subcontinent endemics Salea, Sitana, and Otocryptis.
The Eocene exchange hypothesis
The first Draconinae invasion into India consisted of a lineage represented today by the endemic genus Salea, which descended from a mainland Asian ancestor that also gave rise to the Indochinese genus Calotes. This colonization event most likely resulted from an early Eocene land-bridge connection or an over-water dispersal event just prior to the ISC’s connection with Sundaland (Eurasia) 50–55 MYA (Fig. 3b). Given the sedentary and arboreal natural histories of extant draconine species, we feel the former hypothesis is more likely than the latter, although we acknowledge the possibility of both. We expect a broader sampling within this clade of Southeast Asian, and especially Indian, species will provide a better estimate of the ancestral area at this node (Salea + Calotes: Fig. 3a). The second dispersal event into India occurred with the divergence of the Indian and Sri Lankan endemics Sitana and Otocryptis from an ancestor most likely found in Sundaland during the middle Eocene. This colonization of the Indian subcontinent most likely was facilitated via a land bridge that connected the ISC with Sumatra and the Thai-Malay peninsula at 48 MYA. Additionally, the lineage sister to Sitana and Otocryptis, Japalura, and Pseudocalotes, is Phoxophrys (Fig. 3a). This genus is endemic to the lowland forests of Borneo and Sumatra—further supporting an India-Sundaland (Eurasia) connection via Sumatra and the southern portion of the Thai-Malay Peninsula during the middle Eocene. These independent colonization events not only support Moody’s  pre-collision biogeographic hypothesis, but also give additional phylogenetic support for Eocene land bridges postulated by Acton,  and Ali and Aitchison . Our results contribute to a growing body of literature demonstrating the possibility of floral and faunal exchange between India and Eurasia during the Eocene, before the ISC’s hard collision 20–25 MYA (e.g. freshwater crabs: ; rhacophorid tree frogs: Li et al. ). Given the ecology of these organisms, and of the draconine species sampled here, we feel that it is less likely Eocene faunal exchanges occurred as the result of over water dispersal events. It is unclear whether the Eocene land bridges were two separate spatial/temporal features, versus possibly the same entity, just changing position as the ISC progressed northward. In either case, their existence may have provided continental connections between Southeast Asia and India during the Eocene, which could have allowed for terrestrial exchanges between these areas. These results collectively represent a broad-scale pattern of faunal exchange between the ISC and areas of Eurasia before its collision with Asia, at least partially facilitated by land bridges, which we term the “Eocene Exchange Hypothesis.” Furthermore, we believe the reoccurring and somewhat subjective disagreement between the Indian vs. Asian origins hypotheses [2–12, 16], have simply identified opposing perspectives of a broad geographic and temporal conduit of opportunity for faunal exchange between India and Eurasia. Future studies would benefit from an attempt to empirically focus on the timing and direction of faunal exchange between these biogeographic regions, rather than a prevalence of one scenario over the other.
Revision of the age of draconinae
Our estimate for the age of Draconinae is significantly older than those previously published in broad scale squamate phylogenetic studies (most recently ). Our older estimates are largely due to our consideration of the acrodont fossils, Mimeosaurus and Priscagama, as leiolepids rather than stem agamids, following Estes et al. . These fossils have had a rather turbulent history of classification, with various studies suggesting Mimeosaurus was allied with the Chameleonidae ; then hypothesized to be located along the branch leading to Leiolepis and Uromystax ; and lastly united with Priscagama in an extinct subfamily, Priscagaminae , considered to be a stem lineage of Leiolepis and Uromystax .
This confusion has persisted because when Mimeosaurus and Priscagama were first described, the contemporary genera Leiolepis and Uromystax were still included within the family Agamidae and demonstrated to be the sister group to the remaining agamids  (this relationship has been further confirmed with molecular data [21, 23, 52, 53]. However, Estes et al.  removed Leiolepis and Uromystax from the Agamidae and placed them in their own family (the Leiolepidae), and this taxonomy has not been followed by subsequent studies. Thus, the acrodont fossils of Priscagama and Mimeosaurus have been consistently considered as stem fossils for all agamids and not their sister group, Leiolepis and Uromystax. We followed the taxonomy of Estes et al.  and considered Mimeosaurus and Priscagama as stem leiolepids and not stem agamids. It was this placement that lead to our older estimates of Draconinae origins (85–92 MYA). However, this estimate is consistent with the ages of new amber agamid fossils being described out of Indochina and previous studies on Iguanian lizards (; Bauer et al., unpublished data; personal communication with JLG and PW). We recommend that researchers continue to follow the taxonomy of  with the recognition of the Leiolepidae as a distinct family and the placement of priscagamine fossils as stem to Leiolepis and Uromystax, as suggested in the original descriptions of these fossils [20, 50, 51].
The use of additional taxa, sequence-capture data, and newer geological models—all data not available to previous studies on Draconinae—resulted in novel and well-resolved relationships, leading to new biogeographic insights in this unique subfamily of lizards. Using these biogeographic insights and a broad comparison with previous biogeographic literature, we propose the Eocene Exchange Hypothesis, and the simple but well supported assumption that land bridges may have facilitated a broad-scale pattern of faunal exchange between the ISC and areas of Eurasia before its collision with Asia during the Eocene. We expect that with additional sampling of Indian and mainland Asian species, some factors that may have biased our biogeographic interpretations within the Draconinae to (i.e., Indian extinction events), can be evaluated. In addition, sampling of additional draconine species will allow us to test more fine-scaled hypotheses concerning dispersal and diversification within this group. Our phylogenomic analysis add to a growing body of knowledge addressing the effects of the ISC’s collision on biogeography and offers new ideas to be tested by future studies.
Eocene Exchange Hypothesis
million years ago
For tissues, we thank Bryan L. Stuart, Aaron Bauer, L. Lee Grismer, Jens Vindum (CalAcad.) Jimmy McGuire (MVZ), Funding provided by Clarkson University and NSF through its post-doctoral fellowship program and grants (DEB-9726064, DEB-9982736, and DEB-0451832). For field assistance we thank Indraneli Das and for assistance with UCE pipeline we thank Carl H. Oliveros.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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