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Julian Rowe Dupuis Speciation and hybridization in the Old World swallowtail butterfly (Papilio machaon) species complex by Julian Rowe Dupuis A thesis submitted in partial fulfillment of the requirements for the degree of Doctorate of Philosophy in Systematics and Evolution Department of Biological Sciences University of Alberta © Julian Rowe Dupuis, 2016 Abstract Species delimitation is fundamental to evolutionary biology. However the process is far from straightforward in systems with complex evolutionary histories, and the concept of species as taxonomic hypotheses is often overlooked in many biological disciplines. Here I investigate species delimitation operationally, with a review and meta-analysis of the literature, and empirically, by investigating hybridization in swallowtail butterflies. First, I conducted a literature review on studies that used multiple molecular markers to delimit closely related species of animals and fungi. I evaluated the relative success of different types of molecular markers (mitochondrial, ribosomal, nuclear, and sex-linked genes) in delimiting closely related species and asked whether increased geographic or population-level sampling and the number of markers affected identification success. With this foundation, I then investigated hybridization in the Old World swallowtail butterfly (Papilio machaon Linnaeus, 1758) species complex. At a North America-wide scale, I assessed the putative hybrid origins of multiple lineages in the group, using morphology, mitochondrial DNA, microsatellites, and ecological characteristics. I then focused on a hybrid zone in southwestern Alberta and tested whether population genetic structure of the area (using mitochondrial DNA and microsatellites) was similar to an assessment done 30 years ago using morphology and allozymes. I also compared multiple hybrid identification and classification (F1, F2, backcross) methods for microsatellites and a genome- wide single nucleotide polymorphism dataset for a subset of individuals. Finally, I asked whether environmental or landscape variables could explain variation in genetic differentiation and interspecific hybridization in this hybrid zone, using spatial ecology and landscape genetics methods. This is the first application of raster-based landscape genetics methods to interspecific ii hybridization. Together, the progression of studies in this thesis provide important insight into species delimitation and add to a growing body of research documenting the complexity of hybridization, as well as its potential for generating biodiversity. iii Preface This thesis is an original work by Julian R Dupuis. However, productive science is achieved through collaborations and mentorship; therefore, “we” is used throughout the text of the data chapters as a reflection of those involved. A version of chapter 2 has been published as Dupuis, JR, Roe AD, Sperling FAH (2012) “Multi- locus species delimitation in closely related animals and fungi: one marker is not enough.” Molecular Ecology volume 21, pages 4422-4436. Here I collected data and conceived and conducted analyses, and drafted the original manuscript. ADR helped to collect data and conceive analyses, and FAHS contributed conceptual guidance. All authors contributed analytical guidance and provided input to the manuscript throughout its preparation. A version of chapter 3 has been published as Dupuis JR, Sperling FAH (2015) “Repeated reticulate evolution in North American Papilio machaon group swallowtail butterflies.” PLOS ONE volume 10, e0141882. Here I collected data, conducted data analyses, and drafted the original manuscript, and FAHS contributed conceptual guidance. All authors contributed analytical guidance and provided input to the manuscript throughout its preparation. iv In memory of my father, Earl Bradley Dupuis v Acknowledgements To begin, thank you Felix, for supporting me in innumerable ways over the past several years. Your guidance and encouragement, and support of my random side projects and teaching opportunities, have been integral to my development as a scientist. I look forward to future collaborations (some of which are already started), and many more manuscripts in which to contend my florid writing style. Thank you to my supervisory committee, Jocelyn Hall, Scott Nielsen, and Heather Proctor, for your guidance over the years. I would like to thank John Acorn and Francis Yeh for participating on my candidacy examination committee, and JC Cahill and Andrew Hendry for acting as arms-length and external examiners for my defense. Many people facilitated the research in this thesis. Thanks to Corey Davis and Cheryl Nargang for everything molecular biology, Gary Anweiler, Giovanny Fagua, Monica Higuera, Gerry Hilchie, and Max Larrivée for collecting swallowtails, and Fabien Condamine, Patrick James, Jasmine Janes, Lisa Lumley, Rene Malenfant, and Karina Silva-Brandão for various kinds of technical and analytical help. Thanks to all of the entomologists, lab members, and fellow grad students over the years: Lisa, Jason, Ben, Marla, Alex, Doug, Ronald, Gwylim, Erin, Giovanny, Monica, Evan, Christi (both of you), Jaz, Josh, Rene, Cathy…thanks for all the great memories (my apologies if I missed anyone; you know who you are). And thanks to Boyd and Bryan. Without your continued willingness to “discuss” aspects of this thesis, it would be much drier. Thanks to my family, mom and Eliot, for your love and support despite the few thousand kilometers between us the past few years. Who knew that those first bamboo and coat hanger nets would lead to this? Finally, thanks to Caroline for everything: your love and encouragement, vi for dealing with vials everywhere all the time, allowing the co-opting of our vacations to collect bugs, etc. You’ve brought more to my life, and thus this thesis, than could be put down in writing here. This research was funded by an NSERC Discovery Grant to FAHS, and an Alberta Conservation Association Grant in Biodiversity and a Canadian Circumpolar Institute, Circumpolar/Boreal Alberta Research Grant to myself. vii Table of contents General introduction .....................................................................................................................1 1.1 General introduction ........................................................................................................................... 1 1.2 Thesis overview .................................................................................................................................. 3 1.3 Literature cited .................................................................................................................................... 9 Multi-locus species delimitation in closely related animals and fungi: one marker is not enough ...........................................................................................................................................18 2.1 Summary ........................................................................................................................................... 18 2.2 Introduction ...................................................................................................................................... 19 2.3 Methods ............................................................................................................................................ 22 2.3.1 Multilocus literature survey ...................................................................................................... 22 2.3.2 Fixation and congruence indices ............................................................................................... 23 2.3.3 Population and geographic sampling adequacy ........................................................................ 25 2.3.4 Multilocus power analysis ......................................................................................................... 26 2.4 Results .............................................................................................................................................. 27 2.4.1 Fixation and congruence indices ............................................................................................... 27 2.4.2 Population and geographic sampling analysis ........................................................................... 28 2.4.3 Multilocus power analysis ......................................................................................................... 29 2.5 Discussion ......................................................................................................................................... 30 2.5.1 Species delimitation success compared across marker classes ................................................. 30 2.5.2 Intraspecific variation and geographic sampling adequacy ....................................................... 31 2.5.3 mtDNA, species delimitation, and taxonomy ........................................................................... 34 2.6 Conclusions ...................................................................................................................................... 35 2.7 Literature cited .................................................................................................................................. 42 Repeated reticulate evolution in North American Papilio machaon group swallowtail butterflies .....................................................................................................................................55
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