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THE DISTRIBUTION of GENOMIC DIVERSITY BETWEEN and WITHIN CRYPTIC SPECIES of FIELD VOLES and SURFCLAMS a Dissertation Presented T

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THE DISTRIBUTION of GENOMIC DIVERSITY BETWEEN and WITHIN CRYPTIC SPECIES of FIELD VOLES and SURFCLAMS a Dissertation Presented T THE DISTRIBUTION OF GENOMIC DIVERSITY BETWEEN AND WITHIN CRYPTIC SPECIES OF FIELD VOLES AND SURFCLAMS A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Nicholas Keech Fletcher August, 2020 © 2020 Nicholas Keech Fletcher PATTERNS OF GENOMIC DIVERSITY WITHIN AND BETWEEN CRYPTIC SPECIES OF FIELD VOLES AND SURFCLAMS Nicholas Keech Fletcher, Ph. D. Cornell University 2020 Understanding how genetic diversity is distributed within and between species is a fundamental goal of evolutionary biology and conservation. Cryptic species are an especially interesting challenge to study in this context as they lack the obvious morphological differentiation that provide clues to how genetic diversity may be partitioned. In this dissertation, I analyze genetic diversity in two unique cryptic species groups, voles in the genus Microtus and surfclams in the genus Spisula, at multiple levels of sampling both genomically and geographically. First, I analyze genome-wide single nucleotide polymorphism (SNP) data paired with environmental nice modeling (ENM) to understand how isolation glacial cycling has driven divergence in three cryptic European vole species formerly classified as Microtus agrestis. I find high levels of divergence distributed across the whole genome, with little evidence of ongoing gene flow well as divergence in environmental niches between species. There is a high level of predicted overlap between the niches of M. rozianus and M. lavernedii that has not resulted in any evidence in gene flow between these groups. These cryptic vole species have evolved high divergence across the genome in isolation during glacial cycling. Secondly, I use a dataset including microsatellite markers, mtDNA, and nuclear intron loci to examine patterns of genetic diversity in cryptic subspecies of the Atlantic surfclam, Spisula solidissima. Recently, isolated populations of the lesser- known southern Atlantic surfclam, S. s. similis, were found far north in the range of S. s. solidissima, a commercially important northern subspecies. To test a hypothesis of recency and isolation in the north, this newly found population of S. s. similis was sampled to provide the first population genetic comparison to a population in Georgia, as well as contrasts with S. s. solidissima. These recently discovered northern populations of S. s. similis showed a slight reduction in genetic diversity but high levels of connectivity with southern populations. Genetic differentiation was weak and only significant for microsatellite data. Based on coalescent modeling, I conclude that the northern S. s. similis populations most likely represent a post-glacial expansion, and it is hypothesized that there are unidentified stepping-stone populations connecting populations throughout its range. Finally, I explore a characteristic pattern of genomic variation within many species in Britain, dubbed the Celtic Fringe, which is generated by the two waves of colonization after the Last Glacial Maximum. Here I analyze low-coverage whole genome sequencing and full mitochondrial genomes from 11 populations and 124 individuals of the short-tailed field vole (Microtus agrestis), to explore patterns of genome-wide introgression and divergence across the Celtic Fringe. I find high genome-wide divergence between our northern and southern populations, with a strong signature of isolation by distance north to south. There is also a signature of mito-nuclear divergence in my genetic data, and the southern mitochondrial haplotype has not introgressed as far north as the southern nuclear DNA. I find no signature of selection in the data, and my results point to genetic drift the major evolutionary process driving divergence genome-wide between our populations. This study offers insights into the evolutionary and demographic processes that drive Celtic Fringe patterns in Britain and have led to contemporary patterns of genetic diversity after climatic cycling. BIOGRAPHICAL SKETCH Nicholas (Nick) Keech Halvard Fletcher grew up in southern California, where he went to Corona del Mar High School. His love for the natural world was sparked young and he spent his early days catching “blue bellies” in California and “kopparormar” in Sweden during the summer. Nick graduated from University of California Berkeley with a B.A. in Integrative Biology in 2009. While at Berkeley, he worked with Dr. Jim McGuire, studying the evolutionary genetics of Indonesian gliding lizards in the genus Draco. Nick spent a summer as an undergraduate field tech in western Sumatra and the Mentawai Islands collecting herpetofauna for the Museum of Vertebrate Zoology. He also studied coral rubble-inhabiting crustacean communities in Mo’orea, French Polynesia during a semester-long field course in 2009. After Berkeley, Nick worked as a laboratory technician in Dr. Alicia McDonough’s lab at the Keck School of Medicine at the University of Southern California in Los Angeles. In the McDonough lab he helped investigate salt and potassium homeostasis, kidney disease and hypertension in rat models. Nick joined the Searle lab in the Department of Ecology and Evolutionary Biology at Cornell in 2012 to study evolutionary genomics in small mammals and other organisms. In the last year of his PhD, Nick finished remotely while working as a part-time instructor of Introductory Biology at Montgomery College, Takoma Park/ Silver Spring. He will begin a position as a professional-track instructor in the Department of Biology at the University of Maryland shortly after his PhD. v This dissertation is dedicated to my morfar Dr. Bo Liander (1932-2020), whose love of the natural world and life-long learning inspired me to pursue this PhD. vi ACKNOWLEDGMENTS Firstly, I would like to thank Jeremy Searle for all of his guidance and support as my advisor during my PhD. Without his unwavering generosity and kindness, this dissertation would not be possible. I would also like to thank the rest of my committee: Matt Hare, Jerry Herman and Nina Therkildsen. They provided me with all kinds of support and were just all-around great people to interact with. Special thanks to Rick Harrison, he was a huge influence on my scientific thinking before he passed away and I am still inspired by him. I would also like to acknowledge the other professors in the department who helped me with other aspects of teaching or research: Irby Lovette, Betty McGuire, Michelle Smith, Kelly Zamudio, Harry Greene, Willy Bemis, Monica Geber, Greg Graffin, Jed Sparks, and Brian Powell. I would also like to thank my coauthors on my chapters, who were instrumental in helping my research ideas come together: Pelayo Acevedo, Joana Castro, Paolo C. Alves, and Nicolas Lou. Thank you to the revolving cast of Searle Lab members/visitors past and present who made it a great and supportive place to do research: Ben Johnson, Jacob Tyrell, Henry Kunerth, Jon Hughes, Trevor Sless, Frída Jóhannesdóttir, Soraia Barbosa, Rodrigo Vega, Tom White, Bret Pasch, Alex Gomez- Lepiz, Svetlana Pavlova, Mumtaz Baig, Joanna Stojak, Margherita Collini, Arden Hulme-Beaman, Marja Heikkinen, and Alexandra Trinks. The Hare lab members were my “second family” so thanks to Harmony Borchardt-Weir, Cat Sun, Alyssa Wetterau, Ellen George, Laura Eierman, and Mallory Choudoir. I have been lucky to work with a great group of undergraduate research and teaching assistants so thank you to Nikrumah Frazer, Tamar Law, April Townson, Matthew Sison, Beatriz Olivia, Brianna Mims, Samuel Coleman, Dylan Tarbox, Cassandra Ramirez, Allyson Evans, Brian Magnier, Frank DeAntonio, Camille Mangiaratti, Brian O’Toole, and Mary Margaret Ferraro. EEB has fantastic staff that allows the department to function and vii are great people, thank you Carol Damm, Jennifer Robinson, Patty Jordan, Luanne Kenjerska, John Howell, DeeDee Albertsman, Brian Mlodzinski, Alita Howard, Christine Bogdanowicz, Steve Bogdanowicz, Janeen Orr and Ashley Pendell. The EEB community (and beyond!) of grad students and post docs at Cornell not only provided me with invaluable intellectual and professional feedback, they became some of my best friends. The community is the greatest strength of the department, and I am truly indebted to everyone, but special thanks to (in no order): Nick Mason, Scott Taylor, Laura Porturas, Ann Bybee-Finley, Sahas Barve, Dave Toews, Cait McDonald, Leo Campagna, Roxanne Razavi, Mariah Meek, Cinnamon Mittan, Petra Deane, Michelle Wong, Stepfanie Aguillon, Maria Akopyan, Kara Andres, Amelia Demery, Emily Funk, Olivia Graham, Natalie Hofmeister, Lizzie Lombardi, Anyi Mazo-Vargas, Tram Nguyen, Jasmin Peters, Sue Pierre, Bhavya Sridhar, Young Ha Suh, Katie Sirrianni, Karin Van der Burg, Rachel Wilkins, MG Weber, Gideon Bradburd, Jennie Miller, Arne Jacobs, Lina Arcila Hernandez, Nati Garcia, James Lewis, Will Wetzel, Geoff Giller, Daniel Hooper, Liz Clayton-Fuller, Collin Edwards, Suzi Claflin, Yasir Ahmed-Braimah, and Keeley MacNeill. I want to thank my “new” family: Tip, Blair, and Priscilla Tracy. They have been so welcoming and supportive of me in the last few years of my PhD. I also want to thank my “old” family. Anna and Karl, you are the best siblings I could ever ask for and have tolerated and even encouraged all my animal shenanigans our whole lives. Love you so much. Mom and Dad, you are the most supportive, caring and generous people I know, I hit the jackpot with you two and love you very much. Finally, Allison,
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