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Using Biogeography, Population and Landscape Genetics to Elucidate Patterns and Processes of Diversification in a Biodiversity Hotspot

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Using Biogeography, Population and Landscape Genetics to Elucidate Patterns and Processes of Diversification in a Biodiversity Hotspot Mountains and Migrations: Using Biogeography, Population and Landscape Genetics to Elucidate Patterns and Processes of Diversification in a Biodiversity Hotspot By Chan Kin Onn Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. ______________________________ Chairperson Rafe M. Brown ______________________________ Mark T. Holder ______________________________ Robert G. Moyle ______________________________ Mark Mort ______________________________ Li, Xingong Date Defended: 10 Nov 2017 The dissertation committee for Chan Kin Onn certifies that this is the approved version of the following dissertation: Mountains and Migrations: Using Biogeography, Population and Landscape Genetics to Elucidate Patterns and Processes of Diversification in a Biodiversity Hotspot ______________________________ Chairperson Rafe M. Brown Date Approved: 6 December 2017 ii ABSTRACT Elucidating the tempo and mode of diversification is a major goal of evolutionary biology and represents a fundamental step towards understanding how biodiversity is generated and maintained. Achieving this goal is challenging due to the multidimensional complexity of macro- and micro-evolutionary forces that act across time, space and different phylogenetic levels. Furthermore, these evolutionary forces can involve both adaptive and neutral processes that form confounding interactions with landscape/environmental characteristics. Understanding how genes, geography, and ecology interact to generate, maintain and distribute biodiversity, therefore requires numerous datatypes and analytical resources that span different disciplines such as biogeography, population, and landscape genetics. The primary goal of this study is to provide a better understanding of the patterns and processes involved in the diversification of frogs from the family Ranidae through the use of genomic data and recent advances in analytical methods. Malaysia is one of the most biodiverse and environmentally threatened countries in the world. It is part of Sundaland, a biodiversity hotspot that has undergone dramatic climatic fluctuations in the past few million years. The dynamic geological history, coupled with the highly heterogeneous landscape of Malaysia, provides an ideal system to study the patterns and processes of diversification within a spatial and temporal context. Such studies are of particular importance in Malaysia as it is the country with the highest rate of deforestation in the world. Moreover, most biodiversity research in Malaysia revolves around systematic revisions and species descriptions with relatively few studies focused on understanding the evolutionary underpinnings that generate diversity. This study will fill a significant gap in the region’s iii biodiversity research, especially as it represents the first genomic study on Malaysian amphibians. Chapter 1 examines the broad biogeographic patterns of Ranid diversification at the family and generic level. Using the most comprehensive and robust time-calibrated phylogeny to date, we estimated the timing and patterns of major dispersal events to test the hypothesis that colonization of new geographic areas triggers a concomitant acceleration in diversification rates. Additionally, we determined whether the Eocene-Oligocene extinction event (EOEE) had a significant impact on the diversification of Ranids. Our results showed that the EOEE had no effect on diversification rates; most major dispersal events occurred over a relatively short period of time during the end of the Eocene, and the colonization of new geographic areas was not followed by increased net-diversification. On the contrary, diversification rate declined or did not shift following geographic expansion. Thus, the diversification history of Ranid frogs contradicts the prevailing expectation that amphibian net-diversification accelerated towards the present or increased following range expansion. Rather, our results demonstrate that despite their dynamic biogeographic history, the family Ranidae diversified at a relatively constant rate despite their present high diversity and circumglobal distribution. Chapter 2 compares the efficacy of commonly-used species delimitation methods (SDMs) and a population genomics approach based on genome-wide single nucleotide polymorphisms (SNPs) to assess lineage separation in the Malaysian Torrent Frog Complex currently recognized as a single species (Amolops larutensis). First, we used morphological, mitochondrial DNA and genome-wide SNPs to identify putative species boundaries by implementing non-coalescent and coalescent-based SDMs. We then tested the validity of putative boundaries by estimating spatiotemporal gene flow to assess the extent of genetic iv separation/cohesion among putative species. Our results show that SDMs were effective at delimiting divergent lineages in the absence of gene flow but overestimated species in the presence of marked population structure and gene flow. However, using a population genomics approach and the concept of species as separately evolving metapopulation lineages as the only necessary property of a species, we were able to objectively elucidate cryptic species boundaries in the presence of past and present gene flow. Chapter 3 builds on the findings of the previous chapter to determine the spatiotemporal factors that generated the genetic differentiation in Amolops. We tested the significance and relative contributions of (1) geographic distance (isolation-by-distance, IBD); (2) landscape/environmental variables including mountain ranges, river basins, forest cover, and habitat suitability (isolation-by-environment, IBE); and (3) historical events (isolation-by- colonization, IBC) towards genetic differentiation. Results showed that interspecies diversification was primarily driven by historical events (IBC); IBD was responsible for intraspecies population structure, and IBE did not play a significant role in the diversification of Amolops. Additionally, demographic analyses detected significant population bottlenecks, indicating that speciation was most likely due to founder effect speciation. v ACKNOWLEDGEMENTS I thank the Biodiversity Institute (KUBI), Department of Ecology and Evolutionary Biology (EEB), Graduate Student Organization, National Science Foundation Doctoral Dissertation Improvement Grant (DEB-170203) and National Geographic Society (Grant number 9722-15) for providing support and funding for this dissertation research. I would like to specifically thank the Director of the KUBI Dr. Leonard Krishtalka, the Chair of EEB Dr. Christopher Haufler, the EEB Graduate Coordinator Aagje Ashe, Lori Schlenker and Jamie Keeler at KUBI for their time, patience and technical assistance throughout my time at KU. My committee members Town Peterson, Rob Moyle, Mark Mort, Li Xingong, and especially my major advisor Rafe Brown have been invaluable sources of guidance and support. My graduate career would not have been possible without the support and mentorship of my friend, collaborator, and mentor, Lee Grismer who played a major role in my scientific development. I would like to thank past and present graduate students, and especially members of the herpetology division who have assisted and supported me in various ways: Bill Duellman, Linda Trueb, Rich Glor, Jeet Sukumaran, Jamie Oaks, Charles Linkem, Cameron Siler, Carl Oliveros, Patrick Monnahan, Anthony Barley, Luke Welton, Alana Alexander, Jesse Grismer, Perry Wood Jr., Scott Travers, Karen Olson, Tashitso Anamza, Kerry Cobb, David Blackburn, Luke Mahler, Su Yong Chao, Matt Buehler, Robin Abraham, Carl Hutter, Kevin Chovanec, Pietro de Mello, Katie Allen, Walter Tapondjou, Jeff Wienell, Matt Jones, Javier Torres and Mark Herr. I thank my family who nurtured my love and interest in nature and never once pressured me to pursue anything except that which I am passionate about. Last but not least, I thank my partner in life, Lynn for providing unwavering love and moral support. She, together with our vi dogs Sophie, Tori and Suki have brought joy, balance and sanity to my life when times got difficult. vii CONTENTS TITLE AND ACCEPTANCE PAGE i ABSTRACT iii ACKNOWLEDGEMENTS vi TABLE OF CONTENTS vii DISSERTATION Chapter 1. Spatiotemporal diversification of True Frogs (family: Ranidae): testing the “Dispersification” and Mass-Extinction Hypotheses 1.1 Abstract 1 1.2 Introduction 2 1.3 Methods 1.3.1 Sampling and time-calibrated phylogenetic estimation 4 1.3.2 Ancestral range reconstruction 5 1.3.3 Diversification rate analyses 6 1.4 Results 1.4.1 Sampling and time-calibrated phylogenetic relationships 7 1.4.2 Ancestral range reconstruction 8 1.4.3 Diversification rate-shifts 9 viii 1.5 Discussion 1.5.1 Diversification rates 9 1.5.2 Timing and patterns of diversification 10 1.5.3 Amphibian diversification during the EOEE 11 1.5.4 Systematics 12 1.6 Tables 14 1.7 Figures 15 Chapter 2. Species delimitation with gene flow: a methodological comparison and population genomics approach to elucidate cryptic species boundaries in Malaysian Torrent Frogs 2..1 Abstract 24 2.2 Introduction 25 2.3 Methods 2.3.1 Sampling, data collection and accessibility 29 2.3.2 Establishing putative species boundaries 31 2.3.3 Validation of putative species boundaries using genome-wide SNPs 35 2.4 Results 2.4.1 Phylogenetic relationships 39 2.4.2 Morphological variation and putative species boundaries
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