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The Role of Social and Individual Pathogen Defense in an Insect with Facultative Family Life: Insights Into the Early

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The Role of Social and Individual Pathogen Defense in an Insect with Facultative Family Life: Insights Into the Early The role of social and individual pathogen defense in an insect with facultative family life: insights into the early evolution of group living Dissertation Zur Erlangung des Grades Doktor der Naturwissenschaften Fachbereich Biologie Johannes-Gutenberg Universität Mainz Maximilian Körner geb. am 08. Juni 1985 in Hamburg, Deutschland Mainz, 2018 Dekan: 1. Berichterstatterin: 2. Berichterstatter: Tag der mündlichen Prüfung: 18.12.2018 TABLE OF CONTENTS SUMMARY ............................................................................................................................................................. 2 GENERAL INTRODUCTION ...................................................................................................................................... 4 EARLY SOCIAL EVOLUTION AND THE ROLE OF PATHOGENS CHAPTER 1 ........................................................................................................................................................... 26 FECES PRODUCTION AS A FORM OF SOCIAL IMMUNITY IN AN INSECT WITH FACULTATIVE MATERNAL CARE CHAPTER 2 ........................................................................................................................................................... 46 GROWING UP WITH FECES: BENEFITS OF ALLO-COPROPHAGY IN FAMILIES OF THE EUROPEAN EARWIG CHAPTER 3 ........................................................................................................................................................... 64 THE IMPACT OF MATERNAL CARE ON OFFSPRING GENE EXPRESSION IS LOWERED BY PATHOGEN EXPOSURE IN AN INSECT WITH FACULTATIVE FAMILY LIFE CHAPTER 4 ........................................................................................................................................................... 84 AGE, PATHOGEN EXPOSURE, BUT NOT MATERNAL CARE SHAPE OFFSPRING IMMUNITY IN AN INSECT WITH FACULTATIVE FAMILY LIFE CHAPTER 5 ......................................................................................................................................................... 104 SOCIAL IMMUNITY: WHY WE SHOULD STUDY ITS NATURE, EVOLUTION AND FUNCTIONS ACROSS ALL SOCIAL SYSTEMS CHAPTER 6 ......................................................................................................................................................... 120 CONDITION-DEPENDENT TRADE-OFF BETWEEN WEAPON SIZE AND IMMUNITY IN MALES OF THE EUROPEAN EARWIG CHAPTER 7 ......................................................................................................................................................... 140 EXTENDED WINTERS ENTAIL LONG-TERM COSTS FOR INSECT OFFSPRING REARED IN AN OVERWINTERING BURROW PERSPECTIVES .................................................................................................................................................... 162 THE ROLE OF PATHOGEN PRESSURE IN SHAPING SOCIAL SYSTEMS ACKNOWLEDGEMENTS ...................................................................................................................................... 179 REFERENCES ....................................................................................................................................................... 179 CURRICULUM VITAE........................................................................................................................................... 205 SUMMARY The study of the emergence of group living and its evolution into permanent and complex societal systems is a major topic of interest in evolutionary biology, entailing careful study of the costs and benefits constraining and driving social evolution. One of the most prominent challenges group living species face is an increased risk of pathogen infection. To overcome this threat, individuals in groups can not only increase their investment into personal defenses, such as physiological and behavioral immunity, but also exhibit collective defenses known as social immunity. Recent studies suggest that social immunity plays a key part in the early emergence of sociality – yet little is known about their role in primitive groups, such as facultative family associations. In particular, it remains largely unknown to what degree social immunity in subsocial species is mediated by parental care, or how collective immunity shapes investment into personal immunity in these family groups. In this thesis, I examine these questions in the European earwig Forficula auricularia, an insect exhibiting facultative family life. The first part of this thesis focuses on better understanding the role and effectiveness of social immunity in the European earwig. In Chapter 1, I show that social immunity occurs in this species through antimicrobial activity from the feces excreted by both the caring mother and the offspring. In Chapter 2, I demonstrate that the feces of offspring provide starvation resistance to siblings if no regular food sources are available, suggesting an additional and non-immune related role of feces production. In Chapter 3, I demonstrate that the presence of pathogens does cause offspring to overexpress immunity related genes during family life, but only in absence of a caring mother. Nevertheless, maternal care does not seem to shape offspring immunity long-term: in 2 Summary Chapter 4, my data reveal that the presence of a pathogen, but not of the mother, affects the immunity of earwig offspring in adulthood. Finally, I address the recent findings of social immunity in subsocial species and their implications on social evolution in Chapter 5. In the second part of this thesis, I focused on advancing our understanding of personal pathogen defenses, a critical component in the role and effectiveness of social immunity in social evolution. In particular, we aimed to highlight the difficulty of correctly assessing personal immune investment by investigating insect immune functions in the light of key physiological constraints. In Chapter 6, I showed that larger forceps trade-off with earwig immunity, but only in relatively small earwig males, and only after an immune challenge – overall highlighting the importance of a careful, multipronged approach when measuring immunocompetence. The data presented in Chapter 7 finally shows that shorter winter length during development increases key parts of adult female immunity, but only if specimen were kept with unfamiliar conspecifics, which emphasizes the role of social stresses in immune investment. In conclusion, this dissertation emphasizes how the proposed important redefinition of social immunity sets the stage for future inquiries into the role of pathogen pressure in early social evolution. By also highlighting key trade-offs between individual immunity and physical constraints, my work may lay the groundwork for new perspectives and informed investigations into the crucial interplay of personal immunity, social immunity, and the consolidation of facultatively social individuals into interdependent and complex social systems. 3 GENERAL INTRODUCTION Early social evolution and the role of pathogens Maximilian Körner “Logic clearly dictates that the needs of the many outweigh the needs of the few.” - Mr. Spock, Star Trek II: The Wrath of Khan (1982) General Introduction SINGLE TO SOCIETY: SOCIAL EVOLUTION Throughout the history of life on Earth we find evolutionary changes with an impact so profound that they alter habitats and ecosystems on a global scale. These so-called major transitions in evolution represent the formation of increasingly organized collectives by previously individual actors, such as the rise of multicellular organisms from single cells, or the assembly of individuals to form societal systems (Szathmáry and Smith, 1995). These increases in organizational hierarchy can only occur when conflict between individual elements is absent or suppressed. They therefore do not represent some form of inevitable natural progression in complexity, but rather a contingency depending on the selective conditions at any given point in time (Bourke, 2011). As a result, there is no directional bias, no guarantee life can, must, or will evolve towards the next level of organizational complexity. Understanding the processes and conditions enabling the emergence and maintenance of social structures from independent, solitary individuals is one of the central pillars of evolutionary biology. Sociality can take many forms, ranging from temporary and facultative associations to permanent and obligate societies. These forms are likely to evolve successively, with comparatively simple, subsocial systems transitioning through obligate associations towards highly complex and organized eusocial superorganisms (Bourke and Franks, 1995; Crozier and Pamilo, 1996; Wilson, 1971). The exploration of mechanisms driving these transitions was accompanied by the emergence of inclusive fitness theory, which to this day underlies the core framework of sociobiology by explaining how donors of costly interactions with relatives can reap beneficial returns (Hamilton 1964a; Hamilton 1964b; Frank 1998; Marshall 2015). At the heart of 5 General Introduction this framework lies the rejection of the notion that animals group up because of benefits to the population or species, and the consideration of fitness benefits provided to each individual in a group as the key drivers of sociality (Williams 1966, Hamilton 1971, Korb & Heinze 2015). This realization was crucial, since we can only begin to explore how sociality first emerged and has
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