Forficula Auricularia

Influence of Ecology and Social Interactions on the Early Evolution of Family Life Dissertation Zur Erlangung des Grades Doktor der Naturwissenschaften Am Fachbereich Biologie Der Johannes-Gutenberg Universität Mainz Jos Kramer geb. am 18. November 1985 in Filderstadt, Deutschland Mainz, 2016 Dekan: 1. Berichterstatterin: 2. Berichterstatterin: Tag der mündlichen Prüfung: 17.01.2017 TABLE OF CONTENTS Summary 2 General Introduction 5 Chapter 1. Negative association between parental care and sibling cooperation in 19 earwigs: a new perspective on the evolution of family life? Chapter 2. Maternal condition determines offspring behavior toward family members 39 in the European earwig. Chapter 3. Influences of relatedness, food deprivation, and sex on adult behaviors in 55 the group-living insect Forficula auricularia. Chapter 4. When earwig mothers do not care to share: parent-offspring competition 71 and the evolution of family life. Chapter 5. Short-term benefits, but transgenerational costs of maternal loss in an 89 insect with facultative maternal care. Chapter 6. The population determines whether and how life-history traits vary between 107 reproductive events in an insect with maternal care. Chapter 7. Kin and multilevel selection in social evolution: a never-ending controversy? 123 Perspectives 141 Author contributions 150 Acknowledgements 152 References 153 Curriculum vitae 172 1 SUMMARY A core research area in evolutionary biology is devoted to the investigation of universal mechanisms that drive transitions to social life. The formation of animal societies out of formerly independent, solitary organisms has long taken center stage in the quest for these mechanisms. However, while transitions from family systems to the highly integrated societies of cooperatively breeding vertebrates and eusocial insects have been thoroughly explored, little attention has thus far been paid to the evolutionary origin of the allegedly simple family systems themselves. Hence, the mechanisms promoting the early evolutionary stages of family life remain poorly understood, despite the pivotal role they might play in explaining transitions from solitary to social life. Here, we investigated evolutionary mechanisms shaping the family life of the European earwig Forficula auricularia, a precocial insect with facultative post-hatching maternal care that recently emerged as a model system for the early evolution of family life. In particular, we assessed the impact of social interactions, basic life-history characteristics, and environmental conditions on the costs and benefits of earwig family life, and thus sought to determine how their interplay might affect the evolutionary origin and subsequent consolidation of family life. The first part of this thesis investigates the relationship between different types of social interaction among European earwigs to elucidate potential mechanisms underlying the fitness effects of facultative social life. Chapter 1 shows that the cooperative food transfer among earwig nymphs increases if mothers do not provision their offspring at a sufficiently high level, indicating that sibling cooperation could complement the benefits of facultative parental care in driving the early evolution of family life. Chapter 2 demonstrates that the propensity of earwig nymphs to share food depends on the condition of their mother. Offspring thus seem to flexibly adjust their behavior toward siblings in response to changes in parental care. However, such complex behavioral patterns do not seem to promote gregariousness in adult earwigs; chapter 3 reveals that the intimate social interactions typical for family life only partly extend into the semisocial adult stage. Overall, these results affirm the pre-eminent role of the family (as compared to other types of) group in the evolution of advanced animal societies, and demonstrate that early family systems are not just simplistic imitations of their more advanced counterparts, but rather reflect surprisingly sophisticated social environments in their own right. The second part of this thesis explores how the complex interdependencies of social interactions, basic life-history characteristics, and environmental conditions affect the costs and benefits of facultative family life. Specifically, chapter 4 shows that parent-offspring competition drastically reduces offspring survival under food limitation, suggesting that this mechanism might hamper the evolution of family life under harsh environmental conditions. By contrast, chapter 5 demonstrates that maternal loss unexpectedly increases the body size of offspring, but impairs 2 their expression of parental care in the adult stage – pointing at a crucial role of such long-term costs in the maintenance of early forms of family life. Finally, chapter 6 shows that life-history traits of mothers and their offspring vary between the first and last reproductive event in a partly population-specific manner, indicating that this variation reflects age-dependent changes in parental investment, and population idiosyncrasies that likely arose as the result of different environmental conditions. Altogether, these findings point at a crucial role of the joint effects of environmental conditions and life-history characteristics in the early evolution of family life. Finally, the third part of this thesis takes a broad theoretical perspective, and explores how the study of family life might integrate into the current theory of social evolution. In particular, chapter 7 reviews the enduring controversy surrounding two major theories of sociobiology – kin selection theory and multilevel selection theory – and suggests that both approaches provide different, but complementary perspectives on social evolution that could jointly advance our understanding of evolutionary transitions from solitary individuals to complex animal societies. In conclusion, this dissertation demonstrates that facultative family systems can give rise to surprisingly sophisticated social environments that are shaped by a unique set of behavioral mechanisms, and thus often differ profoundly from the social environments in obligatory family systems. Specifically, sophisticated forms of parental care are here paralleled by sophisticated forms of sibling cooperation, and parents not only confer long-term benefits to their offspring, but also directly compete with them for limited food resources. Importantly, the social behaviors expressed during family life resonate in the behaviors expressed in the adult stage, as well as affect life-history characteristics found across populations. The interplay between all these parameters is ultimately likely to shape the evolution of family life and thus more generally, the transition from simple to complex family systems. 3 GENERAL INTRODUCTION The early evolution of family life Jos Kramer “Furthermore, in many groups of organisms, from the social insects to the primates, the most advanced societies appear to have evolved directly from family units.” Edward Osborne Wilson, 1975. Sociobiology General Introduction TRANSITIONS TO SOCIAL LIFE Throughout the history of life on earth, previously independent units have formed social collectives that allowed them to cope with the numerous challenges imposed by their ever- changing environment: genes grouped together in cells; cells grouped together in multicellular organisms; and multicellular organisms grouped together in societies. Transitions from solitary to social life were the incipient steps in such major transitions in evolution, and hence often had far-reaching repercussions on the diversity, complexity, and hierarchical organization of life itself (Szathmáry and Maynard Smith 1995; Bourke 2011a). On these grounds, the investigation of the mechanisms driving transitions to social life has emerged as a core research area in evolutionary biology (Alexander 1974; Krause and Ruxton 2002; Bourke 2011a). The formation of animal societies out of formerly independent, solitary organisms has long taken center stage in the quest for general mechanisms that drive social evolution. Indeed, it has prepossessed scientists ever since Charles R. Darwin first speculated on the evolution of eusocial societies in his book On the Origin of Species (he suggested that selection at the family-level would resolve his ‘special difficulty’ of explaining the emergence of sterile worker castes; Darwin 1859). Since then, the mechanisms driving transitions from simpler social systems to the highly integrated and often permanent societies of cooperatively breeding vertebrates and eusocial insects have been thoroughly explored (e.g. Wilson 1971; Bourke and Franks 1995; Crozier and Pamilo 1996; Koenig and Dickinson 2004; Koenig and Dickinson 2016). This process was paralleled by the development of inclusive fitness theory, the central theoretical framework underpinning modern sociobiology (Hamilton 1964a; Hamilton 1964b; Frank 1998; Marshall 2015). However, less consideration has been given to the evolutionary origin of the simpler social systems themselves (Trumbo 2012; Falk et al. 2014), and the incipient steps in transitions to social life thus remain poorly understood. Pathways of Group Formation In principle, transitions from solitary to social life in simple (temporary and often facultative) animal societies can roughly follow two different pathways: the semisocial and the subsocial (Michener 1969; Bourke 2011a). The semisocial pathway occurs when group formation results from the aggregation of individuals

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