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Sociality in Cobweb Spiders (Anelosimus Spp.): Evolutionary Consequences and the Role of Pre-Existing Traits

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Sociality in Cobweb Spiders (Anelosimus Spp.): Evolutionary Consequences and the Role of Pre-Existing Traits SOCIALITY IN COBWEB SPIDERS (ANELOSIMUS SPP.): EVOLUTIONARY CONSEQUENCES AND THE ROLE OF PRE-EXISTING TRAITS by Kieran Mikhail Samuk H.B.Sc., University of Toronto, 2008 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) July 2011 © Kieran Mikhail Samuk, 2011 Abstract Sociality – cooperative group living – is ubiquitous in the natural world, yet our understanding of its evolution is still in its infancy. In this thesis, I explore two poorly understood aspects of the evolutionary origin and consequences of sociality using social cobweb spiders (Anelosimus spp.) as a model system. First, I examine how pre-exisiting traits have contributed to the evolution of alloparental care – the care of non-descendant offspring – in social cobweb spiders. I begin by showing alloparental care is extensive in wild social cobweb spider nests. I then test the hypothesis that alloparental care occurs as a result of a lack of discrimination against foreign egg sacs. In support of this hypothesis, I show that subsocial species from clades sister to the social species freely care for foreign egg sacs. This suggests that a lack of offspring discrimination is ancestral to sociality in cobweb spiders. and alloparental care likely emerged spontaneously along with group living. This may have facilitated the evolution of sociality by immediately providing the group-level benefits of alloparental care. Secondly, I examine how social life may have altered natural selection acting on social cobweb spiders. In social cobweb spider nests, the protection offered by a communal nest and the presence of alloparents may have relaxed natural selection on individual maternal care behaviour. Using a comparative approach, I test the hypothesis that sociality is associated with reduced maternal care behavioural phenotypes. I show that social species from independently derived social clades score significantly lower than their subsocial sister taxa on six different assays of maternal care, including the probability of repairing damaged egg sacs and of abandoning egg sacs in the face of simulated predation. Integrating a number of supporting facts, I interpret this result as suggestive of relaxed natural selection on maternal care behaviour as a consequence of sociality. Together, the two comparative studies I present reveal a key role for pre-existing traits in the origin of sociality and that the forces of evolution are likely altered in concert with the onset of social life. ! ii ! Preface I played the lead role in the two projects described in Chapters 2 and 3 of this thesis. Along with my supervisor Dr. Leticia Avilés, I conceived and designed the project described in Chapter 2. I performed all field and laboratory work, statistical analyses, preparation of figures, and writing. Gyan Harwood (University of British Columbia) assisted with field and laboratory work. Dr. Avilés helped review and provide comments on the resulting chapter. Chapter 3 was based on a project I had a lead role in conceiving and designing, along with my supervisor. I carried out all fieldwork, statistical analyses, writing and preparation of figures. Emily LeDue (Dalhousie University, second co-author of Chapter 3) and myself performed the laboratory work. Dr. Avilés again helped review and provide comments on the resulting chapter. ! iii ! Table of contents Abstract ............................................................... ii Preface ............................................................... iii Table of contents ....................................................... iv List of tables ............................................................ v List of figures .......................................................... vi Acknowledgments ...................................................... vii Chapter 1: General introduction Introduction ...................................................... 1 Contents and aims of this thesis ....................................... 5 Chapter 2: Evidence for the emergent origin of alloparental care in social cobweb spiders Introduction ...................................................... 7 Methods ........................................................ 11 Results ......................................................... 16 Discussion ...................................................... 17 Chapter 3: Sister clade comparisons reveal reduced maternal care behaviour in social cobweb spiders Introduction ..................................................... 28 Methods ........................................................ 31 Results ......................................................... 36 Discussion ...................................................... 37 Chapter 4: General conclusion Summary of findings .............................................. 50 Future studies .................................................... 53 Conclusion ...................................................... 54 References ............................................................ 56 Appendices Appendix A: Simulation of estimate accuracy in alloparental care assays ...... 75 Appendix B: The effect of paint marks on spider care behaviour ............. 82 Appendix C: Pairwise tests of maternal behaviour care contrasts ............ 84 ! iv ! List of tables Table 2.1 Effect of maternity on four measures of maternal care in Anelosimus ....... 24 Table 3.1 Comparisons of maternal care between subsocial and social Anelosimus .... 46 Table B.1 The effect of egg sac paint marks on maternal care in Anelosimus ......... 83 Table C.1 Pairwise tests of maternal care behaviour contrasts ..................... 84 ! v ! List of figures Figure 2.1 Two pathways for the evolution of alloparental care ................... 25 Figure 2.2 The extent of alloparental care in six species of Anelosimus ............. 26 Figure 2.3 Plots of differences in the level of five Anelosimus care behaviours ........ 27 Figure 3.1 Maternal care measured in natural nests of six species of Anelosimus ...... 47 Figure 3.2 Probability of accepting and repairing egg sacs in six species of Anelosimus . 48 Figure 3.3 Probability of dropping or reclaiming egg sacs in six species of Anelosimus .. 49 Figure A.1 Simulation of estimated rates of egg-sac switching vs. number of females ... 77 ! ! ! ! ! vi ! Acknowledgements This thesis could not have been completed without the help and support of many amazing people. First and foremost, I am grateful to my supervisor, Leticia Avilés. Her skillful guidance, knowledge and enthusiasm made working in her laboratory truly a pleasure. Secondly, my committee members Wayne Maddison and Dolph Schluter provided many helpful and insightful comments throughout the process that greatly improved this thesis. Many thanks also to members of the Avilés lab: Jennifer Guevara, Gyan Harwood, Jessica Purcell, Maxence Salomon and Ruth Sharpe, for (1) willingly reading and commenting on early versions of my manuscripts with little to no coercion and (2) being fantastic lab mates, field companions and friends. I am also deeply grateful to all the incredible, intelligent and hilarious members of Zoology and Botany Departments at UBC. Doing science at UBC is a pleasure and a privilege, and I could not ask for better colleagues and friends. Thanks especially to Aleeza, Alana, Andrea, Brook, Dave, Gerald, Gina, Greg, Jasmine, Jon, JS, Kate, Kathyrn, Matt, Laura, Leithen, Rich, and Sam for many helpful scientific and statistical discussions and general awesomeness. I am extremely thankful for the financial support provided to me during my degree by the Natural Sciences and Engineering Research Council of Canada (NSERC) and UBC. NSERC funded most of the research in this thesis through a Discovery Grant to Dr. Avilés, and a CGS-M to myself. I would further like to thank the staff of SIMBIOE and El Ministerio del Medio Ambiente de Ecuador for assistance with logistics and obtaining permits, and for the opportunity to do field work in beautiful Ecuador. The associates of Reserva Ecólogica Antisana, Estacion Biológica Jatun Sacha and Bellavista Cloudforest Reserve also all provided fantastic general assistance and field support. Special thanks also to Maurico Vega and Gabriel Iturralde, whose generous help with field work in Ecuador was invaluable to the success of this thesis. Finally, and most importantly, thank you to my family for supporting and inspiring me always. ! vii ! Chapter 1 General introduction Sociality, i.e. cooperative group living, has long intrigued biologists. This interest may be somewhat self-reflective: humans are, after all, social animals. That said, the ecological importance and success of social animals is undeniable. Social insects, for example, constitute around 75% of the world’s insect biomass (Holldobler & Wilson 1990). The evolutionary impact of sociality is also widely acknowledged. The transition to social life is often accompanied by profound morphological change, the evolution of novel behaviours, and the alteration of life histories (Keller 2009). In short, sociality has played an important role in shaping both organisms and the ecosystems they inhabit. Accordingly, understanding how sociality arises has become a major focus of evolutionary research over the past fifty years (Foster 2010). Current approaches Thus far, two complementary approaches have dominated the study of the evolution of sociality. The first
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