Integrating Phylogenomics, Biogeography and Systematics to Explore the Taxonomy and the Rise of the Ratsnakes
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City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 2-2015 Integrating phylogenomics, biogeography and systematics to explore the taxonomy and the rise of the ratsnakes Xin Chen Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/541 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] Integrating phylogenomics, biogeography and systematics to explore the taxonomy and the rise of the ratsnakes by Xin Chen A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2015 © 2015 Xin Chen All Rights Reserved ii This manuscript has been read and accepted by the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. Dr. Frank T. Burbrink Chair of Examining Committee Dr. Laurel A. Eckhardt Executive Officer Dr. Michael J. Hickerson Supervisory Committee Dr. Ana C. Carnaval Supervisory Committee Dr. R. Alexander Pyron Supervisory Committee Dr. Christopher J. Raxworthy Supervisory Committee The City University of New York iii Abstract Integrating phylogenomics, biogeography and systematics to explore the taxonomy and the rise of the ratsnakes by Xin Chen Advisor: Dr. Frank T. Burbrink Understanding the evolutionary processes that create the spectacular diversity of organisms, both in species numbers and form, is a primary goal for biologists. Global ratsnakes are a species-rich assemblage with high morphological and ecological diversity and a distribution that encompasses both the Old World (OW) and the New World (NW). To explore the mechanism leading to the divergence of the ratsnakes, I tested the hypotheses regarding the area of origin and global dispersal, and examined the patterns of diversification and trait evolution. Given adaptive radiation via ecological opportunity, a diversity-dependent diversification pattern and an early burst trait evolutionary pattern are expected with rapid divergence triggered by the appearance of new resources, extinction of competitors, colonization of new areas or the appearance of key innovations. Thus, I tested if the radiation of ratsnakes follows diversity- dependent diversification with an early burst in speciation and trait divergence and whether the iv variation in diversification is associated with OW-NW dispersal or changes in traits. Further, trait convergence between OW and NW lineages was investigated to determine, if given similar environmental conditions, rapid speciation via ecological opportunity is repeatable. To answer the questions mentioned above, a robust phylogenetic tree is fundamental. Due to potential gene tree/species discordance, hundreds of loci sampled across the entire genome were generated using the anchored hybrid enrichment approach and the multi-species coalescent methods were used to build the species phylogeny. Then, given this phylogenetic context, taxonomic changes were made to reflect named monophyletic groups and divergence time and ancestral areas were estimated to 1) infer the processes leading to the current ratsnake global distribution, 2) assess the best fitting diversification and trait evolution models, and 3) determine if ecomorphological convergence occurs with adaptive regimes of traits on the phylogeny. Among all of the inferred species trees, by comparing the extent of tree discordance and the gene tree errors, the species trees generated in the program MPEST with summary statistics of posterior probability gene trees was used for further analysis. First, it was determined that the traditional ratsnake genera Gonyosoma and Coelegnathus are excluded from the monophyletic ratsnake group, with the remaining monophyletic group defined as Coronellini. The reconstructed ancestral areas supported that ratsnakes originating in the OW Eastern Palearctic and with a single dispersal to the NW via Bergingia. Two subclades each defined by a single genus, Lampropeltis and Elaphe, were found to have exclusively elevated species diversification and trait evolutionary rates. As the rate accelerations were only in the recent divergent lineages, colonization to the NW and rapid speciation of the NW lineages were decoupled. A general diversity-dependent radiation pattern in both OW and NW lineages was supported with a recent sharp diversification elevation about 6.5 Ma mainly within the genera Lampropeltis and Elaphe. Three morphological v convergence events were detected among OW and NW lineages, corresponding to the previously defined morphological taxonomies (i.e., Elaphe and Pantherophis), indicating without a robust molecular phylogeny, morphological convergence positively misleads taxonomy. This research demonstrates the advantages and challenges of phylogenetic inference using genome scale dataset, highlights the importance of incorporating the biogeographic history and trait evolution in studies of diversification and indicates that oversimplified models are insufficient to describe the complexity of processes shaping the diversity in a species-rich assemblage. vi Acknowledgments I would like to thank my dissertation committee members Drs. Michael J. Hickerson, Ana C. Carnaval, R. Alexander Pyron, Christopher J. Raxworthy, and especially my dissertation advisor, Dr. Frank T. Burbrink, whose support and advisement made this study possible. Thank you to all past and present members of the Burbrink Lab (E. Myers, S. Ruane, A. McKelvy, J. Burgoon, T. Guiher, A. Kuhn), who have helped me in countless ways. I would also like to thank the following for providing tissues, specimens and support during this project: American Museum of Natural History (D. Frost, C. Raxworthy, D. Kizirian, J. Feinstein, R. Pascocello) Louisiana State University Museum of Natural Sciences (J. Boundy, D. Dittman, R. Brumfield, F. Sheldon), Museum of Vertebrate Zoology (J. McGuire, C. Spencer), Smithsonian Institution National Museum of Natural History (A. Wynn, J. Jacobs), California Academy of Sciences (J. Vindum, D. Blackburn, R. Lawson), University of Kansas Biodiversity Institute (R. Brown, A. Barley, A. Campbell), Museum of Comparative Zoology – Harvard University (J. Rosado), Royal Ontario Museum (R. Murphy, R. MacCulloch), University of Colorado Museum of Natural History (M. Kageyama, C. McCain,), Chengdu Institute of Biology – Chinese Academy of Sciences (J. Li, Y. Wang, S. Li), Kunming Institute of Zoology – Chinese Academy of Sciences (D. Rao, J. Wang), Museo de Zoologia "Alfonso L. Herrera" Universidad Nacional Autonoma de México (A. Nieto Montes de Oca), The Field Museum (K. Kelly, A. Resetar), M. Brandley, K. Jiang, L. Ding, P. Guo, S. Huang, J. Che, Y. Zhang, H. Zhao, W. Dong, H. Takeuchi, W. Wüster, Z. Nagy, D. Mulcahy, Y. Wu, W. Huang, vii X. Hua, Y. Zeng, J. Zhang, J. Grummer, J. Goldenberg. L. Liu, T. Shaw, Z. Ruan, J. Brown, J. Ash, R. Chaudhary, A. Lemmon, E. Lemmon, L. Grismer, M. Matsui, K. Nishikawa, R. Strobel. Funding for this research was provided in part by PSC-CUNY, CUNY Graduate Center Doctoral Student Research, US NSF Grant DBI-0905765 to R.A.P. and L. Clampitt, S. Harris and D. Rosenberg. This research was also supported, in part, by the National Science Foundation Grants CNS-0958379 and CNS-0855217 and the City University of New York High Performance Computing Center. viii Table of Contents Pages Introduction 1-7 Chapter 1: The repeatedly unidirectional dispersal from the Old 8-15 World to the New World in advanced snakes forms the intercontinental distribution of ratsnakes Chapter 2: Species diversity of ratsnakes part I – The phylogenetic 16-24 position and taxonomic status of the Rainbow Tree Snake Gonyophis margaritatus (Squamata: Colubridae) Chapter 3: Species diversity of ratsnakes part II – Assessing species boundaries and the phylogenetic position of the rare Szechwan 25-38 ratsnake, Euprepiophis perlaceus (Serpentes: Colubridae), using coalescent-based methods Chapter 4: The ratsnake species tree inferred using 100's of loci and 39-64 multi-species coalescent methods Chapter 5: Relating ecological and trait convergence to species 65-94 diversification and the biogeographic areas of origin in ratsnakes Tables 95-104 Figure Legends 105-109 Figures 110-130 Appendices 131-200 Literature Cited 201-223 ix List of Tables Pages Table 1.1 Time calibrations and the tree prior distribution used for divergence time 95 estimation in BEAST 1.6.2. Table 2.1 Species synonymized into the genus Gonyosoma. 96 Table 3.1 The species delimitation results using Bayes Factor model selection approaches. 97 Table 3.2 Currently recognized ratsnake species. 98-100 Table 4.1 The results of pairwise species tree comparisons. 101-102 Table 5.1 The best-fit diversification models. 103 Table 5.2 Phylogenetic signals and best-fit evolutionary models for multiple phenotypic 104 traits and ecological traits. x List of Figures Pages Figure 0.1 The global distribution of ratsnakes. 110 Figure 1.1 Dated phylogeny representing main families and subfamilies in Colubroidea. 111 Figure 2.1 The time-calibrated phylogeny including 101 taxa. 112 Figure 3.1 The distribution of species in genus Euprepiophis. 113 Figure 3.2 The species tree estimated using *BEAST. 114 Figure 4.1 Categories