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Evolutionary Ecology of Host-Parasite Interactions in the Trinidadian Guppy (Poecilia Reticulata)

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Evolutionary Ecology of Host-Parasite Interactions in the Trinidadian Guppy (Poecilia Reticulata) Evolutionary ecology of host-parasite interactions in the Trinidadian guppy (Poecilia reticulata) Felipe Pérez-Jvostov Institute of Parasitology McGill University Montreal, Quebec A thesis submitted to McGill University in partial fulfillment of the requirements of the Degree of Doctor of Philosophy! ! © Felipe Pérez-Jvostov, 2015 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 A mi familia, Felipe, Victoria, Karina y Sabrina. ! ii! I shall always feel respect for every one who has written a [dissertation], let it be what it may, for I had no idea of the trouble which trying to write common English could cost one –! CHARLES R. DARWIN, Letter to W. D. Fox, 1837 ! iii! THESIS ABSTRACT Some of the most extraordinary examples of adaptive evolution are the result of the interactions between hosts and their parasites. Although this so-called arms race between host defense and parasite virulence can have direct implications for host fecundity and survival, current research shows that parasitic infections can also change host behavioral and physiological traits. Hosts face multiple threats at any give time. Other natural enemies like predators and competitors can also reduce host survival. Thus, host-parasite adaptations may not only influence non-host species, but may, simultaneously, be influenced by their interaction with other natural enemies. The role of parasites in modulating multi-species interactions has received increased attention recently, yet the majority of examples come from single case studies. The aim of this dissertation is to fill this gap by using a model organism in evolutionary biology: the Trinidadian guppy. First, I start by broadly differentiating between generalist and specialist parasites, and review the mechanisms by which both can influence non- host species at ecological and evolutionary time scales. This distinction has been extensively studied in relation to the evolution of virulence, but its ecological relevance has been largely neglected. Second, I consider how the particular interactions between guppies and their specialist ectoparasite, Gyrodactylus, are influenced by guppy adaptation to predation (high vs. low) across multiple rivers in Trinidad. I found strong, and repeatable, differences between guppies from different rivers and their capacity to limit Gyrodactylus infections, but found no differences between predation environments. iv ! Nonetheless, a consistent reduction in the growth of guppies exposed to Gyrodactylus was evident, potentially due to the energetic cost associated with the activation and maintenance of an immune response to fight Gyrodactylus infections. These results suggest a divergence in guppy-Gyrodactylus coevolutionary trajectories among rivers (higher resistance and higher virulence vs. lower resistance and lower virulence), and highlight that population evolutionary history (i.e., genetic makeup, founder effects, genetic bottle necks, etc.), and not predation, strongly influence the intensity and direction of host-parasite coevolution in this system. Finally, I explore how Gyrodactylus can modify the interaction between guppies and their natural enemy, Rivulus hartii. I found that although Gyrodactylus can strongly reduce guppy growth, infection does not significantly modify guppy-Rivulus interactions, particularly because guppies can fine- tune their phenotype when simultaneously facing multiple enemies. These results demonstrate that hosts have the capacity to mediate, and even mitigate, any potential ecological effects that parasites could have on the broader community. Understanding the mechanisms by which parasites can influence non-host species has become a major goal in evolutionary ecology. However, the complexity of natural communities, environmental heterogeneity, and host evolutionary history can have strong, and many times unexpected, effects on host-parasite interactions. The results I present here are a vivid example of such a natural community. Using a combination of experimental work and field manipulation, I demonstrate that Gyrodactylus can have strong effects on host life-history traits, but that these effects do not necessarily influence non-host species, largely because of host capacity to limit such effects. I believe my work v ! has laid the foundations for future research on the ecological relevance of Gyrodactylus, as I was the first to investigate how guppy-Gyrodactylus coevolution could potentially influence the coexisting fauna. vi ! RÉSUMÉ DE LA THÈSE Les interactions entre les hôtes et leurs parasites représente un des exemples les plus extraordinaires de l’évolution adaptative. Bien que cette prétendue "course aux armements" entre la défense de l'hôte et la virulence parasitaire puisse avoir des répercussions directes sur la fécondité et la survie de l'hôte, la recherche actuelle démontre que les infections parasitaires peuvent également modifier les traits comportementaux et physiologiques des hôtes. À tout instant, les hôtes doivent affronter une abondance de menaces. Un ensemble varié d’ennemis naturels, tels que les prédateurs et les compétiteurs peuvent également menacer la survie de l'hôte. Ainsi, les adaptations hôte-parasite peuvent non seulement influencer les espèces non hôtes, mais peuvent à la fois être influencées par leur interaction avec d'autres ennemis naturels. Au fil des dernières années, le rôle particulier des parasites qui modulent les interactions multiespèces a fait l'objet d'une attention accrue. Cependant, la majorité des exemples analysés proviennent d'études de cas simples. La présente thèse a pour objectif de combler cette lacune en employant un organisme modèle en biologie évolutive: le guppy trinidadien. Tout d'abord, je commence en caractérisant de manière générale les différences entre les parasites généralistes et spécialistes, pour ensuite envisager les mécanismes par lesquels chacun peut influencer des espèces non hôtes sur des échelles de temps écologiques et évolutives. Cette distinction a déjà été amplement étudiée par rapport à l'évolution de la virulence, mais sa pertinence écologique a été largement négligée. En second lieu, je considère la façon dont les interactions particulières entre les vii ! guppys et leurs ectoparasites spécialistes - soit les Gyrodactylus - sont influencées par l'adaptation du guppy à la prédation (haute versus basse) au sein de plusieurs rivières du Trinidad. Cette approche a dévoilée des différences importantes et répétées entre les populations guppy de différentes rivières et leur capacité de restreindre les infections Gyrodactylus, sans toutefois permettre de constater de différences entre les environnements de prédation. Néanmoins, une diminution constante de la croissance des guppys exposés à Gyrodactylus était évidente, potentiellement en raison des coûts énergétiques associés au déclenchement et à la maintenance d'une réponse immunitaire pour combattre les infections Gyrodactylus. Ces résultats suggèrent une divergence entre les trajectoires coévolutionnaires guppy-Gyrodactylus entre rivières (à savoir une plus grande résistance et une virulence plus élevée versus une faible résistance et un niveau de virulence inférieur), et mettent en évidence que l’histoire évolutive des populations (c’est-à-dire la composition génétique, les effets fondateurs, les goulots d'étranglement génétiques, etc.), et non la prédation, influencent considérablement l'intensité et la direction de la coévolution hôte-parasite de ce système. Enfin, je considère comment le Gyrodactylus peut modifier l'interaction entre le guppy et son ennemi naturel, Rivulus hartii. Bien que Gyrodactylus puisse fortement réduire la croissance guppy, j’ai trouvé que ce dernier ne modifie pas de manière significative les interactions guppy-Rivulus, notamment en raison du fait que les guppys peuvent affiner leur phénotype lorsqu’ils doivent simultanément affronter plusieurs ennemis. Ces résultats démontrent que les hôtes détiennent une capacité de médiation, et même d'atténuer les effets écologiques potentiels que les parasites pourraient avoir au sein de la communauté plus large. viii ! La compréhension des mécanismes par lesquels les parasites peuvent influencer les espèces non hôtes est devenu un objectif capital dans le domaine de l’écologie évolutive. Cependant, la complexité des communautés naturelles, l'hétérogénéité de l'environnement, et l’histoire évolutive de l’hôte peuvent chacun exercer des effets importants et parfois imprévus sur les interactions hôte-parasite. Les résultats de la présente thèse représentent une illustration frappante d'une telle communauté naturelle. En déployant une combinaison de travail d’expérimentation et de manipulation sur le terrain je démontre que Gyrodactylus peut avoir des effets importants sur les traits d'histoire de vie des guppy, mais que ces effets n’influencent pas nécessairement les espèces non-hôtes, notamment en raison de la capacité de l’hôte de limiter ces effets. Attendu qu’aucune étude actuelle ne propose une analyse de l’impact de la coévolution guppy-Gyrodactylus sur la faune coexistante, je crois que ce travail a posé les bases pour de futures recherches portant sur à la pertinence écologique de Gyrodactylus. ix ! TABLE OF CONTENTS THESIS ABSTRACT ........................................................................................................................... iv RÉSUMÉ DE LA THÈSE ..................................................................................................................
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