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Dissertation Jasmin Ruch Hamburg, 2014 EVOLUTION AND MAINTENANCE OF SOCIALITY IN CRAB SPIDERS (THOMISIDAE) Dissertation zur Erlangung des Doktorgrades an der Fakultät für Mathematik, Informatik und Naturwissenschaften im Fachbereich Biologie der Universität Hamburg und der Science Fakultät im Fachbereich Biologie der Macquarie University vorgelegt von Jasmin Ruch aus Buchholz in der Nordheide Hamburg, 2014 EVOLUTION AND MAINTENANCE OF SOCIALITY IN CRAB SPIDERS (THOMISIDAE) Thesis presented for the Doctor of Philosophy/Doctor rerum naturalium to be jointly awarded by Macquarie University and University of Hamburg presented by Dipl. Biol. Jasmin Ruch Hamburg, 2014 Tag der “Oral Defence” an der Universität Hamburg: 08.07.2014 Vorsitzender: Prof. Dr. Andreas Schmidt-Rhaesa Gutachter: Prof. Dr. Jörg Ganzhorn Gutachter: Prof. Dr. Thomas Hoffmeister Dissertationsgutachter: Prof. Rebecca Kilner Dr. Kathrin Dausmann Dr. Mary Whitehouse Prof. Yael Lubin Dissertation freigegeben am 27.11.2014 durch HDR Examination Coordinator Jane Kim (Macquarie University) Table of Contents Summary ......................................................................................................................................... 1 Zusammenfassung.......................................................................................................................... 3 Certificate of originality ................................................................................................................ 5 Acknowledgements..........................................................................................................................9 Chapter 1: General Introduction ..................................................................................................... 11 Chapter 2: Re-description of Xysticus bimaculatus Koch, 1867 (Araneae, Thomisidae) and characterization of its subsocial lifestyle ......................................................................................... 19 Chapter 3: Multiple origins of subsociality in crab spiders (Thomisidae) ..................................... 37 Chapter 4: Mating behaviour and natural mating rates in a subsocial spider ................................ 59 Chapter 5: Offspring dynamics affect food provisioning, growth and mortality in a brood-caring spider ................................................................................................................................................ 73 Chapter 6: Families hunt more successfully: effect of group composition on hunting and communal feeding ............................................................................................................................................. 87 Chapter 7: Hunted hunters? Effect of group size on predation risk and growth in the Australian subsocial crab spider Diaea ergandros............................................................................................103 Chapter 8: General Discussion.......................................................................................................121 Appendix 1: Cuticular Antifungals in Spiders: Density- and Condition Dependence....................131 Summary In this thesis I investigated factors that may explain the evolution and maintenance of sociality in crab spiders (Thomisidae). Group-living crab spiders differ from most other social spiders because they lack a capture web, a factor considered to be very important for the evolution of sociality in spiders. Colonies of subsocial and social spiders are usually comprised of family members, and thus another unusual trait of subsocial crab spiders is the regular acceptance of unrelated conspecifics into their groups. Previous work on the subsocial crab spider Diaea ergandros has demonstrated that maternal care as well as the construction and occupation of nests as protective retreats are important factors that may explain group-living in this species. Furthermore, it has been shown that these spiders are able to recognize kin, which offers an excellent opportunity to study group dynamics between relatives and immigrants. Building up on this knowledge, I examined potential costs and benefits of group living with a focus on the effect of unrelated spiderlings. Moreover, I estimated the genetic relatedness within family groups, and studied the broader natural history as well as phylogenetic relationships of subsocial and social crab spiders. With a detailed natural history description of the crab spider Xysticus bimaculatus I have demonstrated that lifestyle and demographics are very similar to the subsocial Diaea ergandros (chapter 2). This new discovery of subsocial behaviour outside the genus Diaea indicated that subsociality may have evolved multiple times independently within Thomisidae. Testing this hypothesis, I investigated the evolutionary history of social behaviour in crab spiders in a molecular- phylogenetic context. The results suggest that subsociality has at least two independent origins confirming thatX. bimaculatus is not closely related to any of the other group-living thomisid species (chapter 3). The evolution of sociality in spiders is accompanied by a switch from outbreeding to inbreeding. D. ergandros has been suggested to be at a particularly advanced transitory stage from subsocial to social behaviour, and a previous study has shown that populations are inbred. Considering that low mating rates and inbreeding favour offspring cooperation of highly related individuals, females may benefit from monogamous or even incestuous mating. I studied the mating behaviour ofD. ergandros and investigated natural mating rates with microsatellite markers (chapter 4). However, mating trials did not provide evidence for female choice. Accordingly, the genetic analyses did not support the existence of a monogamous mating system but rather supported relatively low mating rates, which may still sufficiently secure offspring cooperation while simultaneously providing some degree of outbreeding. Genetic relatedness has been identified as an important factor promoting cooperation in many subsocial spiders and other organisms studied to date. With two laboratory experiments (chapter 5 & 6) I confirmed that siblings of Diaea ergandros had an advantage over mixed groups that included immigrants. The latter were generally accepted but negatively affected female-offspring and offspring-offspring foraging interactions. Nevertheless, accepting immigrants may have benefits 1 as well. In another experiment, larger groups of D. ergandros outperformed small groups in that they built larger protective retreats and had a lower mortality as well as higher individual growth (chapter 7). Group size varies considerably under natural conditions and small groups may thus benefit from accepting immigrants. 2 Zusammenfassung In meiner Doktorarbeit habe ich Faktoren untersucht, die die Evolution und den Erhalt von Sozialverhalten bei Krabbenspinnen (Thomisidae) erklären könnten. Die meisten subsozialen und sozialen Spinnen bauen große Fangnetze, mit denen sie große Beutetiere überwältigen können und der Bau dieser Netze als gemeinsame Jagdinvestition gilt als ein wichtiger Faktor, der den Erhalt von Sozialitat bei Spinnen erklärt. Anders als die meisten sozialen Spinnen bauen Krabbenspinnen aber keine Netze zum Beutefang. Ein weiterer wichtiger Unterschied zwischen gruppenlebenden Thomisiden und anderen sozialen Spinnen ist in den Verwandtschaftsverhältnissen innerhalb der Gruppen zu finden. In der Regel sind bei subsozialen und sozialen Spinnen die Gruppenmitglieder nah miteinander verwandt und Kooperation zwischen den Individuen wird mit indirekten Fitnessvorteilen erklärt. Subsoziale Krabbenspinnen akzeptieren aber auch nicht-verwandte Artgenossen in ihren Gruppen und unterscheiden sich somit auch in dieser Hinsicht von den meisten anderen subsozialen und sozialen Spinnen. Frühere Studien an der subsozialen Krabbenspinne Diaea ergandros haben gezeigt, dass mütterliche Fürsorge und das Konstruieren und Bewohnen von Blattnestern, die als Zufluchtsort dienen, wichtige Faktoren sind, die das Gruppenleben in dieser Art erklären könnten. Des weiteren wurde gezeigt, dass Individuen dieser Art in der Lage sind, Verwandte von Nicht-Verwandten zu unterscheiden. Daher eignet sich diese Art besonders gut, um die Auswirkung von nicht-verwandten Einwanderern auf die Gruppendynamik zu erforschen. Den Fokus auf die Auswirkung von nicht-verwandten Einwanderern legend, konnte ich somit auf den Ergebnissen vorheriger Studien aufbauen und mögliche Kosten und Nutzen des Lebens in Gruppen bei Krabbenspinnen untersuchen. Darüber hinaus habe ich die genetische Verwandtschaft innerhalb natürlicher Familiengruppen erforscht, die allgemeine Naturkunde dieser Spinnen untersucht sowie die phylogenetischen Verwandtschaftsverhaltnisse von subsozialen und sozialen Krabbenspinnen rekonstruiert. Mit der detaillierten Beschreibung der Naturgeschichte der Krabbenspinne Xysticus bimaculatus konnte ich zeigen, dass diese Art in Bezug auf ihren Lebenszyklus und ihre Demographie der subsozialen Krabbenspinne Diaea ergandros sehr ähnelt (Kapitel 2). Diese neue Entdeckung von subsozialem Verhalten außerhalb der Gattung Diaea deutete an, dass Subsozialität bei Krabbenspinnen mehrfach unabhangig entstanden sein könnte. Daher habe ich die Wurzeln des Sozialverhaltens bei Krabbenspinnen in einem molekular-stammesgeschichtlichen Kontext untersucht. Diese Studie hat bestätigt, dass X. bimaculatus nicht näher mit den anderen gruppenlebenden Krabbenspinnen verwandt ist (Kapitel 3)
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