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Chapter 2: Mate Choice & Selection

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Chapter 2: Mate Choice & Selection The interaction between natural and sexual selection and the maintenance of biological diversity: From diversification to speciation Amy K. Schwartz Department of Biology McGill University, Montreal December 2009 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctor of Philosophy © Amy Schwartz 2009 All rights reserved. This work may not be reproduced in whole or in part, by photocopy or other means, without permission of the author. i ABSTRACT Speciation involves the reduction of gene flow between populations resulting in reproductive isolation. Natural selection can be a strong promoter of this process when populations in different environments diverge in traits relevant for reproductive compatibility. If such traits are involved in mate choice or recognition, sexual selection is further implicated. Speciation is theoretically most likely when natural and sexual selection act in concert; but both the extent to which this occurs, and which factors mediate this interaction remain unclear. This thesis examines the relative roles of natural and sexual selection during adaptation, and their potential for eliciting reproductive isolation. A quantitative review shows that divergence in sexually selected traits between populations does not predict the magnitude or likelihood of reproductive isolation. Instead, variation in the strength of reproductive isolation depends on the opportunity for gene flow and the nature of selection acting on the traits. Similar results were found in an empirical test of this interaction in Trinidadian guppies (Poecilia reticulata). Populations from different environments do show mating isolation to some degree, but only against geographically proximate, and potentially maladapted, migrants. Together, this suggested that selection on mating preferences is not necessarily coupled with selection on mating traits. An introduction experiment that transplanted guppies into a new environment confirmed this intuition, as female preferences do not appear to respond predictably to broad-scale ecological differences. An opportunity to further examine phenotypic responses to environmental change was afforded with a human alteration of the forest surrounding guppy habitat. Clear-cutting likely influences the way visual signals are maintained, perceived and transmitted. However, spatial and temporal variation in male colour was shown to be independent of the light environment, and is instead likely to be maintained by subtle microhabitat and demographic fluctuations. In summary, this thesis shows that sexual and natural selection can be powerful promoters of diversification between populations, but whether or not this results in speciation depends largely ii on the geographic context, the genetic covariance between male and female mating traits, and the strength of selection acting on each. This work further highlights the importance of considering feedbacks between evolutionary and ecological processes in order to understand the evolution of, and establish the correct targets for the preservation of biological diversity. iii RÉSUMÉ Le processus de spéciation implique une réduction du flux génique entre des populations, et se complète quand le processus de reproduction les isole. La sélection naturelle peut être un important promoteur de ce processus quand les traits responsables de la compatibilité des populations pendant la reproduction divergent. Si ces traits sont impliqués dans le choix du partenaire, la sélection sexuelle est également impliquée. Théoriquement, la spéciation est plus probable quand les sélections naturelle et sexuelle agissent simultanément, mais la prévalence de ce processus et les éléments qui régissent cette interaction ne sont toujours pas clairs. Cette thèse examine les rôles respectifs de la sélection naturelle et la sélection sexuelle au cours de l'adaptation, et des conditions qui mènent à l'isolement reproductif. Une analyse quantitative montre que la divergence des traits sexuels secondaires entre des populations ne prédit ni la quantité, ni la probabilité d'isolement reproductif. Par contre, la variation de l'isolement reproductif entre les taxons dépend de la magnitude du flux génique et du genre de sélection qui agit sur les traits. Des résultats comparables ont été trouvés dans un test empirique de cette interaction avec les guppys de Trinidad (Poecilia reticulata). Les populations qui habitent dans des environnements différents démontrent un certain niveau d‟isolement pour l'accouplement, mais seulement contre les immigrants potentiellement mal adaptés qui proviennent des environs. Par conséquent, la sélection sur les préférences sexuelles qu‟expriment les femelles pour une série de traits chez les mâles n‟est pas nécessairement associée à la sélection sur les traits des mâles. Une expérience où les guppys étaient introduits dans un nouvel environnement a confirmé cette intuition: les préférences des femelles ne semblent pas répondre aux différences écologiques à grande échelle, ni aux traits des mâles. Une autre occasion d‟étudier les réponses phénotypiques aux changements environnementaux s‟est présentée lorsque la forêt aux environs de l‟habitat d‟une population de guppys a été altérée. La coupe à blanc peut influencer la façon dont les signaux visuels sont maintenus, perçus et transmis. Cependant, la variabilité spatiale et temporelle de la couleur des mâles est indépendante de l'environnement lumineux, mais elle est susceptible aux iv fluctuations démographiques et des microhabitats. En résumé, cette thèse montre que la sélection sexuelle et la sélection naturelle peuvent être des promoteurs puissants de la diversification entre les populations. Que ce processus de diversification mène à la spéciation dépende largement du contexte géographique, de la covariance génétique entre les caractères des mâles et des femelles, et de la force de sélection agissant sur chacun d‟eux. Ce travail met également en évidence l'importance de considérer les boucles de rétroactions entre les processus évolutifs et écologiques afin de comprendre l'évolution et d'établir des objectifs appropriés pour préserver la diversité biologique. v ACKNOWLEDGMENTS Although specific contributions to the work are acknowledged at the end of each chapter, the whole is more than a sum of its parts and would not have been possible without the support, guidance and dedication of certain individuals. First, I thank my supervisor, Andrew Hendry for allowing his knowledge, his confidence, his humility, and his enthusiasm to be so contagious throughout my graduate career. I could not have asked for a better editor: one who can consistently read between my (sometimes) jumbled lines, and catch my (common) lack of visual perspective. I could not have asked for a better mentor: providing ample space to think and the freedom and confidence to follow through on my thoughts, while maintaining a firm and close whip to make sure I developed thought into action. It‟s been my privilege to grow as scientists together. Funding was gratiously provided by the Vineberg Family scholarship, a doctoral fellowship from the Fonds Québecois de Recherche sur la Nature et les Technologies (FQRNT) and Discovery grants from the Natural Sciences and Engineering Research Council (NSERC) to A.Hendry. I‟m extremely grateful to members of the Hendry lab and collaborators whose core has always been one of support. Particular thanks go to those in the formative years that helped shape my perspective: Erika Crispo, Nate Millar, Jean-Sébastien Moore, Katja Räsänen, and Dylan Weese. Thanks also to current and recent members for useful discussion, argument and new perspectives: Daniel Berner, Joey DiBattista, Cristian Correa, Luis deLeon, Renaud Kaeuffer, Joost Rayemaekers and Xavier Thibert-Plante. Although no-one in the Hendry lab can avoid feeding a fish at least once, the following individuals went above and beyond to ensure the survival and fecundity of hundreds of guppies. Special thanks to fellow graduate students Swanne Gordon, Ann McKellar and Maryse Boisjoly who shared the responsibility of the guppy lab. Thanks also to the many volunteers and undergraduate students, especially: Sara Elhajoui, Laura Easty, Zaki Jafry, Artur Kondrash‟ev, and Anil Patel. I‟m particularly grateful to the staff of McGill‟s vi phytotron facility - Mark Romer, Claire Cooney and Frank Scopeletti, for welcoming fish into the greenhouse and responding to every bizarre whim or temperature adjustment I requested without hesitation. Thank you to the graduate students, faculty and staff of the Biology department and Redpath museum for fostering an environment of true collaboration, creativity and freedom for intellectual curiousity. I was also lucky to find true friends in those hallways that inspired me and comiserated with me when I needed it most: Jeremiah Busch, Rod Docking and Anneli Jokela. I am particularly grateful to Lisa Jones who started on this path and changed through it beside me, all along with great understanding and great strength. Finally, I had the good fortune of being able to do my PhD work surrounded by family and a family of friends. Their weekly traditions and regular distractions have kept me grounded, but their unconditional confidence in me have kept me focused on the prize. This thesis is dedicated to all of „my people‟. Thank you. vii CONTRIBUTION OF AUTHORS This thesis consists of versions four manuscripts that are in press, in review or in preparation for submission to journals for
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