Phylogenetic and Experimental Evidence for an Evolutionary Precursor to Male Colouration in Poeciliid Fishes and Their Relatives by Michael Ryan Foisy A thesis submitted in conformity with the requirements for the degree of Master of Science Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Michael Ryan Foisy 2017 Phylogenetic and Experimental Evidence for an Evolutionary Precursor to Male Colouration in Poeciliid Fishes and Their Relatives Michael Ryan Foisy Master of Science Department of Ecology and Evolutionary Biology University of Toronto 2017 Abstract In many animals, phenotypic diversity in males originates through sexual selection. However, the evolutionary origins of female preferences are unclear. The sensory bias hypothesis suggests female preferences can originate as a byproduct of natural selection operating on sensory systems in non-sexual contexts, like foraging. Despite over 25 years of investigation, fundamental tenets of the sensory bias hypothesis remain unresolved. We explicitly test one of these tenets: the historical dependency of male traits on pre-existing biases in females. We marry phylogenetic comparative methods and behavioural experiments to test for this dependency in poeciliids and related fishes. Our results demonstrate that female biases for long-wavelength colours drove the evolution of long-wavelength colouration in males. In addition to demonstrating this dependency, our study suggests (i) behaviour can be phylogenetically conserved, and (ii) natural selection may be the ultimate explanation for a tremendous amount of variation that has classically been attributed to sexual selection. ii Acknowledgments My highest gratitude goes out to my supervisors, Helen Rodd and Luke Mahler, for their limitless patience and enthusiasm. I am thankful for their guidance and for giving me enough line to take this project into greater depths, while still reeling me in when I was in too deep. I am grateful for the opportunity to have travelled so much for my experimental work, which lent to all sorts of interesting experiences including: eating alligator in Texas, hiking in California, and catching amphisbaenids orchid bees in Trinidad. Really, I could not have had better supervisors. Thank you for everything. I have many friends and colleagues to thank for helping me along the way. Rebecca Schalkowski, du warst die erste Freundin, die ich in Toronto gemacht habe. Ich bedanke mich für deine Unterstützung, deine aufrichtige Freundschaft, und für gelegentlich Gespräche auf Deutsch. I would also like to thank: Augustin Le Bouquin for curious conversations and sharing your aesthetic views of the world; James Boyko for constantly debating science with me, and for not getting upset after it took me five months to realize that your name was not “David”; Charlotte for chatting to me about bees at a frequency no one else could possibly tolerate; the ROMulans for sneaking me into the collections and exhibitions; Viviana Astudillo-Clavijo and Melanie Massey for an incredibly beautiful card; Isabela Borges e Eduardo Gutierrez por sua amizade e apoio, e por me ensinar a fazer comida brasileira; Alex DeSerrano and Mitchel Daniel for teaching me how to work in a fish lab and conduct the behavioural experiments; the Rodd lab and work studies for helping care for the fishes; Phylo club for being a fun phylogenetics family who taught me a lot; Christopher Boccia, Luke Owen Frishkoff and the rest of the Mahler lab for teaching me about macroevolution; Jeremy Beaulieu, for developing these super cool methods, and for responding to the barrage of e-mails I’ve sent you over the past year; Markita Savage and Cristina Mendoza at the Xiphophorus Genetic Stock Center for their generosity and assistance iii with the xiphophorine experiments; Gita Kolluru for generosity and guidance with the Girardinus experiments in California; Charles and Susie Clapsaddle, and their family at Goliad Farms, for providing an unparalleled opportunity to test my model, for teaching me about the surrounding plants and towns, and for making me carnitas; Arcadio Valdez-Gonzalez for collaborating and testing several species of Goodeidae; Bill Cole for cold beers and good laughs; Kitty Lam for being an administrative superwoman; Locke Rowe, Heather Proctor, Mike Ryan, Deborah McLennan, and Aneil Agrawal for insightful discussions and feedback on my work; Ben Sandkam for measuring disc reflectance and ambient light spectra; Stephen Wright for letting me run simulations on the grandiflora server; Corlett Wood and Julia Kreiner for help with R; David Punzalan and Alex DeSerrano for help with SAS; and lastly, the Toronto Transit Commission for keeping streetcars (despite their horrible inefficiency), which provided a charming environment for reading and editing papers. We thank NSERC for funding to MRF (NSERC CGS M), DLM and FHR (NSERC Discovery grants). iv Table of Contents Acknowledgments .......................................................................................................................... iii Table of Contents .............................................................................................................................v Chapter 1 Background on Sexual Selection, Especially Sensory Bias ............................................1 Background .................................................................................................................................1 Chapter 2 Phylogenetic and Experimental Evidence for an Evolutionary Precursor to Male Colouration in Poeciliidae and Their Relatives ..........................................................................8 Introduction .................................................................................................................................8 Methods and Results .................................................................................................................11 2.1.1 Phylogenetic test for a precursor underlying male colouration .............................11 2.1.2 A phylogenetic precursor underlies the evolution of male colouration .................12 2.1.3 Experimental tests of the precursor-2 model .........................................................13 2.1.4 The precursor is a pre-existing long-wavelength bias in males and females .........14 Discussion .................................................................................................................................16 Conclusion ................................................................................................................................22 References ......................................................................................................................................27 Appendix A – Supplemental Methods ...........................................................................................38 Appendix B – Supplemental Figures .............................................................................................50 Appendix C – Supplemental Tables ..............................................................................................61 v Chapter 1 Background on Sexual Selection, Especially Sensory Bias The main body of your thesis begins here. Background Charles Darwin (1859, 1871) was the first to propose the concept of sexual selection. He drew inspiration from gaudy male traits, like the peacock’s tail, which were too costly to be explicable under traditional Darwinian evolution. So, Darwin intuited sexual selection (1859, pg. 117), and later on (1871), laid out two central tenets of his theory: (i) males may evolve costly traits (i.e., “armaments”, like antlers) to gain access to females, and (ii) females may evolve preferences for particular male traits (i.e., “ornaments”, like brilliant colouration). These two principles were the foundation of most modern work on sexual selection, and provide a robust explanation for much of life’s rich and beautiful phenotypic diversity. But it wasn’t always this way. While Darwin’s hypothesis that males evolve costly traits to gain access to females was readily accepted, his suggestion that females evolve preferences for particular male traits was passionately rejected by scientific authorities at the time (Wallace, 1895, 1889; Huxley, 1938; reviewed in: Cronin, 1991). This was likely because the notion that female choice could sculpt the direction of male evolution clashed with cultural biases prevalent in 19th-century Victorian society (Cronin, 1991), and because leading biologists were skeptical that females could impose a potent selective force on males (Wallace, 1895, 1889; Huxley, 1938). Ultimately, this rejection set the study of female preferences into a state of torpor, causing the early study of sexual selection to be almost entirely male-centric (Cronin, 1991; Jones & Ratterman, 2009; Parker & Pizzari, 2015). Despite this bias, the field developed insights about many aspects of reproduction including: parent and sex roles, male-male competition, armament 1 and ornament evolution, territoriality and mating strategies, and mating system evolution (Andersson, 1994). Focus eventually shifted away from males (Bateson, 1983; Andersson, 1994), however, and our understanding of the role of female preferences in evolution by sexual selection improved dramatically during the 20th century (reviewed in: Andersson and Simmons, 2006; Kokko et al., 2006; Jones & Ratterman, 2009). Ronald Fisher was one of the first to push back against the