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The Influence of Host Social System on Hostparasite Evolutionary Dynamics

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The Influence of Host Social System on Hostparasite Evolutionary Dynamics The influence of host social system on host- parasite evolutionary dynamics Dissertation submitted for the degree of Doctor of Natural Sciences Presented by Antoon Jacobus (Jaap) van Schaik at the Faculty of Sciences Department of Biology Date of the oral examination: October 5, 2016 First supervisor: Martin Wikelski Second supervisor: Gerald Kerth Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-370734 Towards an understanding of host-parasite evolutionary dynamics in a social world using bats and ectoparasites as a model system. Supported by funding from: Contents Summary 1 Zusammenfassung 3 Chapter 1: General Introduction 8 Host-Parasite dynamics 12 Sociality and parasites 15 Simplifying the complexity: bat-ectoparasite model system 19 Research aims 24 Dissertation outline 26 Chapter 2: Host social organization and mating system shape parasite transmission opportunities in three European bat species 28 Abstract 30 Introduction 31 Methods 36 Results 40 Discussion 46 Supplementary materials 52 Chapter 3: The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts 56 Abstract 58 Introduction 59 Methods 64 Results 71 Discussion 82 Supplementary materials 87 Chapter 4: Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species 92 Abstract 94 Introduction 95 Methods 100 Results 107 Discussion 113 Supplementary materials 118 Chapter 5: Synthesis and general discussion 122 Host sociality and parasite infection dynamics 123 Host sociality and parasite population genetic structure 125 A brief aside on the evolution of virulence and parasite induced restrictions to host sociality 128 Overall impact of host social system on host-parasite evolutionary dynamics 131 Future directions 132 List of publications and selected abstracts 135 Bibliography 141 Author contributions 160 Acknowledgements 161 Curriculum vitae 163 Summary Parasites are ubiquitous in nature, and increased parasite pressure is one of the fundamental costs of sociality. In addition, sociality also affects host- parasite dynamics directly and indirectly at both ecological and evolutionary timescales. At the ecological level, host social contact shapes parasite infection intensity and transmission opportunities, while behavioural and social avoidance mechanisms allow hosts to reduce overall parasite pressure. On an evolutionary scale, the influence that host social system has on parasite genetic structure and the reciprocal selection pressure imposed by each species on the other can strongly influence the evolutionary outcome of host-parasite interactions. Although the role of host social system in shaping parasite infection dynamics is widely acknowledged, its additional role in shaping parasite genetic structure, and thereby influencing the evolutionary dynamics between the two interacting species, is comparatively understudied. In this dissertation, I use a multi-host multi-parasite comparative framework to explore the effects of host social system, and its interplay with parasite life history, on parasite infection dynamics and population genetic structure. Host-parasite dynamics are shaped by myriad factors including the abiotic and biotic environment, host and parasite life history and host social system. This complexity can be considerably reduced when studying permanent parasites, which do not leave their hosts, as the direct interaction between the parasite and the environment is limited. Furthermore, by investigating permanent parasites of closely related hosts with comparable life histories, it becomes possible to directly assess the effect and interaction between facets of host social system and specific parasite life history traits. European bats of the genus Myotis, and two of their common, permanent ectoparasites (wing-mites of the genus Spinturnix, flies of the genus Basilia), offer an ideal model to study this interaction. All host species share a similar life history, but differ in numerous aspects of their social system, including female colony size, male sociality, mating system and the degree of aggregation in winter. Likewise, while both permanent parasites of their bat hosts, the parasites differ in several key life history traits, most notably their reproductive rate and generation time. By using these species in a comparative framework, these differences in host social system and parasite life history can be exploited to attempt to elucidate the effect of individual social and life history traits. Specifically, I 1) characterize the effect that differences in host social system has on mite infection and transmission 1 dynamics, 2) compare the genetic structure of the mites of two bat species to explore the effects of host social system traits on parasite genetic structure, and 3) compare the genetic structure of a mite and fly species both infecting a single host species, to explore the interaction between parasite life history traits and host social system. Regarding parasite infection and transmission dynamics (chapter 2), I found substantial differences in mite infection intensity across three bat hosts, which correlated closely with the degree of sociality (aggregation size) of both host sexes. Additionally, the transmission rate of the different mite species was strongly correlated to the degree of contact between the sexes afforded by their differing mating systems. These differences at the ecological level also had readily visible effects on mite population genetic structure (chapter 3). In a comparison of population genetic structure between Spinturnix bechsteini and S. myoti, I found large differences in the level of genetic differentiation between, and degree of genetic turnover within, individual mite populations. These differences again closely correlated to those predicted based on host aggregation size and mating system. Finally, in a comparison of mite and fly population genetic structure on a single host (chapter 4), I showed that parasite reproductive rate and generation time interact with seasonal changes in host social organization to yield highly divergent genetic structures. In both investigations of parasite population genetic structure, the differences observed between parasite species were much larger than expected, and have significant implications for the evolutionary potential and the evolutionary trajectory of the host- parasite interaction. These differences are additionally remarkable given the narrow range of host social systems and parasite life histories that were investigated, emphasizing the effect that even subtle differences in facets of either host or parasite can have. Taken together, these results provide a compelling example of the influence of host social system in shaping host-parasite dynamics at both ecological and evolutionary timescales. In doing so, they contribute to our general understanding of the fundamental factors underlying the structure and function of animal sociality. Notably, understanding host-parasite eco- evolutionary dynamics additionally has direct conservation applications as it may aid in combatting emerging infectious diseases, as well as help understand the effects of the numerous ways in which anthropogenic change alters the social system and population dynamics of host animals. 2 Zusammenfassung Die Allgegenwärtigkeit von Parasiten in jeder Form des sozialen Zusammenlebens stellt einen der grundlegendsten Nachteile sozialer Systeme dar. Enger Kontakt führt zwangsläufig auch zu einer größeren Parasitenbelastung und somit zu höheren Kosten für die Wirtsart. Zusätzlich beeinflusst soziales Verhalten die Ökologie und die Evolution der Interaktionsdynamik zwischen Wirt und Parasit sowohl direkt als auch indirekt. Auf ökologischer Ebene stellen Sozialkontakte eine Möglichkeit der Übertragung für nicht mobile Parasiten dar, der die Wirtsart mit Anpassung ihres Verhaltens sowie dem Vermeiden bestimmter Kontakte entgegenwirken kann. Im evolutionären Maßstab gesehen können sowohl der Einfluss des Sozialverhaltens der Wirtsart auf die genetische Struktur des Parasiten als auch der gegenseitige Selektionsdruck zwischen Wirt und Parasit einen enormen Einfluss auf das entwicklungsgeschichtliche Ergebnis von Wirt- Parasit Interaktion haben. Obwohl die Rolle unterschiedlicher Sozialsysteme von Wirtsorganismen als entscheidend für die Infektionsdynamik einer zugehörigen Parasitenart anerkannt sind, wurde der Einfluss verschiedener Sozialsysteme auf die genetische Beschaffenheit der entsprechenden Parasiten-Populationen und die damit einhergehende Einwirkung auf die evolutionäre Dynamik zwischen Wirt und Parasit jedoch bislang größtenteils vernachlässigt. In dieser Dissertation analysiere ich den Einfluss sozialer Wirtssysteme auf den Lebenszyklus, die Infektionsdynamik und die genetische Struktur der entsprechenden Parasitenarten mit Hilfe eines mehrere Wirts- sowie Parasitenarten umfassenden Vergleichsrahmen. Die Interaktionsdynamik zwischen Wirt und Parasit wird von unzähligen Faktoren beeinflusst, so zum Beispiel von abiotischen und biotischen Umweltfaktoren, vom artspezifischen Lebenszyklus von Wirt und Parasit, sowie vom Sozialsystem des Wirts. Parasitenarten, die dauerhaft auf ihrer Wirtsart verbleiben, bieten sich daher zum Studium solcher Systeme besonders an, denn der unmittelbare Kontakt zwischen Parasit und Umwelt ist stark eingeschränkt und somit gestaltet
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