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Parallel Divergence by Allochrony and Cryptic Speciation in Two

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PARALLEL DIVERGENCE BY ALLOCHRONY AND CRYPTIC SPECIATION IN TWO HIGHLY PELAGIC SEABIRD SPECIES COMPLEXES (HYDROBATES SPP.) By Rebecca Sarah Taylor A thesis submitted to the Department of Biology in conformity with the requirements for the degree of Doctor of Philosophy Queen’s University Kingston, Ontario, Canada December 2017 Copyright © Rebecca Sarah Taylor, 2017 Abstract Sympatric speciation, the evolution of reproductive isolation between populations without physical barriers to dispersal, is less likely than allopatric speciation due to the need to overcome potentially homogenizing gene flow. Cryptic species - two or more species mistakenly classified as one usually due to morphological similarity - can form in allopatry or sympatry. One potential mechanism of cryptic speciation in sympatry is allochronic speciation, i.e. divergence driven by differences in breeding time. In this thesis, I first collated examples where allochrony caused divergence between populations to glean new insights into drivers of shifts in breeding time across taxonomic groups and the genetic underpinnings involved, and to create a framework for future investigations. Using both genetic and genome-wide sequencing techniques, I then investigated drivers of cryptic divergence and the evolution of allochronic populations across the global breeding ranges of two cryptic seabird species complexes, Leach’s and band-rumped storm-petrels (Hydrobates spp.). In Leach’s storm-petrels, I found non-physical barriers to be stronger drivers of divergence than physical ones, with some genetic differentiation between ocean basins but higher differentiation among colonies in the Pacific Ocean. Phylogenetic reconstruction revealed that Guadalupe seasonal populations likely speciated allochronically. In band- rumped storm-petrels, colonies in different ocean basins were genetically differentiated, however phylogenomic reconstruction placed South Atlantic colonies as sister to Pacific colonies, and revealed strong genetic structuring within ocean basins, again suggesting non- physical barriers as drivers of divergence. Band-rumped storm-petrels consist of seven reciprocally monophyletic groups, and thus likely represent up to seven different species. I then investigated whether allochronic populations of band-rumped storm-petrel formed due to a mutation shifting breeding time in a founder event, standing genetic variation ii " at the population level, or plasticity in breeding time. My findings indicate breeding season changes are unlikely to have involved a mutation and founder event, however further work is needed to tease apart the potential roles of standing variation and plasticity. Altogether, this thesis reveals the importance of non-physical barriers to gene flow in Leach’s and band- rumped storm-petrels, uncovers cryptic species needing taxonomic and conservation consideration, and furthers our knowledge of allochronic divergence, an underappreciated mechanism of cryptic diversification. iii " Co-Authorship and Manuscripts Chapter 2: The role of allochrony in speciation Authors: Rebecca S. Taylor and Vicki L. Friesen Molecular Ecology (2017) 26: 3330-3342. DOI: 10.1111/mec.14126. The article was conceived by Vicki L. Friesen and myself. I researched and wrote the manuscript, which was then edited by Vicki L. Friesen. Chapter 3: Sympatric population divergence within a highly pelagic seabird species complex (Hydrobates spp.) Authors: Rebecca S. Taylor, Anna Bailie, Previn Gulavita, Tim Birt, Tomas Aarvak, Tycho Anker-Nilssen, Daniel C. Barton, Kirsten Lindquist, Yuliana Bedolla-Guzmán, Petra Quillfeldt and Vicki L. Friesen Journal of Avian Biology (2017). DOI: 10.1111/jav.01515. I produced microsatellite and mitochondrial sequence data for one subspecies, did all analyses and wrote the manuscript. Anna Bailie and Previn Gulavita undertook lab work to produce most of the microsatellite and mitochondrial sequence data. Tim Birt aided with lab work. Tomas Aarvak, Tycho Anker-Nilssen, Daniel C. Barton, Kirtsen Lindquist and Petra Quillfeldt undertook remote field work to collect samples for this manuscript. Yuliana Bedolla-Guzmán edited the manuscript. Vicki L. Friesen conceived the study, aided with analysis and edited the manuscript. Chapter 4: Cryptic speciation and parallel allochronic divergence within a seabird species complex (Hydrobates spp.) Authors: Rebecca S. Taylor, Mark Bolton, Annalea Beard, Tim Birt, Petra Deane-Coe, Andre F. Raine, Jacob González-Solís, Stephen C. Lougheed, and Vicki L. Friesen iv " Molecular Ecology (in review). Submitted August 2017. Will be re-submitted with revisions early 2018. I conducted field work on Ascension Island to help with sample collection, did most lab work for the ddRADseq data and cytochrome b data, and a portion of the lab work for the mitochondrial control region sequence data. I analysed all data and wrote the manuscript. Mark Bolton, Annalea Beard, Petra Deane-Coe, Andre F. Raine, and Jacob González-Solís helped conceive the study and conducted field work, Tim Birt and Petra Deane-Coe conducted some lab work and both contributed useful discussion, Stephen C. Lougheed aided with the analysis of data and provided intellectual input, and Vicki L. Friesen conceived the study, provided intellectual input and helped edit the manuscript. Chapter 5: The role of plasticity in the evolution of allochronic populations of band- rumped storm-petrel (Hydrobates spp.) Authors: Rebecca S. Taylor, Stephen C. Lougheed, and Vicki L. Friesen In prep. I conducted all lab work, analysed the data and wrote the manuscript. Stephen C. Lougheed helped edit the manuscript and provided valuable discussion, and Vicki L. Friesen conceived the study, provided intellectual input and helped edit the manuscript. v " Acknowledgements Firstly, thank you to my supervisor Vicki Friesen for guiding me through my PhD. Her support has improved my skills both as a researcher and as a scientific writer, but she has also been a mentor to me above pure academic guidance. I would not be as strong and independent a researcher without her help over the last four years. I would also like to thank Stephen Lougheed for welcoming me into his lab. His additional support as a second mentor and research collaborator during this process has been invaluable. I would like to thank my committee members Fran Bonier, Virginia Walker and Scott Lamoureux for challenging me throughout, but also for their feedback, support and encouragement. Special thanks to Tim Birt for help in the lab and as a collaborator on multiple parts of my thesis. I would like to thank lab members who have helped both academically, but also in your support and friendship over the years. In particular, Amanda Cicchino, Anna Tigano, Bronwyn Harkness, Drew Suave, and Nick Cairns, who helped make my PhD experience what is was. I would also like to thank the major collaborators on my project who have been invaluable for guidance and sample collection, especially Mark Bolton for his knowledge and enthusiasm, and Jacob González-Solís for allowing me to work so closely with him and his lab. Thank you to everyone who has helped me in the field, especially Herculano Dinis, and Freyja Montali for an experience of a life time. And thanks to all those people who came to the rescue when field work was not as planned: Brian Cumming, Kim McCauley, Katherine Lemmon, the school of graduate studies, Queen’s International Centre, the British Consulate, the Portuguese Consulate, Kate Montali and Sarah Ryan (aka mum), and of course Freyja for being there with me through the disaster. vi " I would like to thank the many other collaborators and sample collectors, without whom this thesis would not have been possible, with a special mention to Annalea Beard, Will Miles, Andre Raine, Petra Deane-Coe, Anna Bailie, Previn Gulavita, Tomas Aarvak, Tycho Anker-Nilssen, Daniel C. Barton, Kirsten Lindquist, and Petra Quillfeldt with whom I have interacted personally. Thanks also to the funding sources: NSERC, Darwin Plus, Ontario Trillium scholarship, American Ornithologists Union Student Research Hesse Award, and the U.S. Fish and Wildlife Service. Last, but certainly not least, I would like to thank my friends for keeping me sane (you know who you are), and of course my family for being there for me - Sarah Ryan, Elizabeth Anderson, Jemma Thompson, Ben Taylor, Charlotte Cousins, Rachel Dunigan, and Mark Taylor. In particular, I dedicate this thesis to my mum, Sarah Ryan, as well as to Jemma Thompson and Ben Taylor, for your extreme level of support during my insane number of years as a student - you are the only reason I have survived it, and I promise I am done now! vii " Statement of Originality I hereby certify that all of the work described within this thesis is the original work of the author. Any published (or unpublished) ideas and/or techniques from the work of others are fully acknowledged in accordance with the standard referencing practices. Rebecca Sarah Taylor (December, 2017) viii " Table of Contents Abstract ................................................................................................................................... ii Co-Authorship ....................................................................................................................... iv Acknowledgements ................................................................................................................ vi Statement of Originality ....................................................................................................
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  • Molecular Phylogenetics and Evolution 94 (2016) 47–54

    Molecular Phylogenetics and Evolution 94 (2016) 47–54

    Molecular Phylogenetics and Evolution 94 (2016) 47–54 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogenetic analysis of the winter geometrid genus Inurois reveals repeated reproductive season shifts q ⇑ Satoshi Yamamoto a, , Eugene A. Beljaev b, Teiji Sota c a Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada, Kobe 657-8501, Japan b Institute of Biology and Soil Science, Prospect 100 Let Vladivostoku 159, Vladivostok 690022, Russia c Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan article info abstract Article history: Winter geometrid moths belonging to the genus Inurois comprise nine species that reproduce during Received 12 March 2015 early winter, three species that reproduce in late winter, and polymorphic species with genetically Revised 15 July 2015 diverged early and late winter populations that co-occur widely across the species’ range. In our previous Accepted 17 August 2015 studies, we demonstrated that differences in reproductive timing resulted in allochronic reproductive Available online 22 August 2015 isolation between sympatric populations. In the present study, to assess the evolutionary pattern of reproductive timing within the genus, we determined the phylogenetic relationships among species Keywords: using nuclear and mitochondrial gene sequences. Nuclear gene tree showed that reproductive season Allochronic speciation shifts occurred independently in four of 13 divergence events. In two divergence events, allochronic sister Introgressive hybridization Parallel divergence lineages were formed in sympatry, suggesting that the segregation of the reproductive season was asso- Temporal isolation ciated with diversification in the genus Inurois.