MATING TRAIT DIVERGENCE IN HABRONATTUS AMERICANUS JUMPING SPIDERS AND SEX RATIO EVOLUTION UNDER SEXUAL CONFLICT by Gwylim Seaton Blackburn BSc., University of British Columbia, 1997 MSc., Simon Fraser University, 2004 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (ZOOLOGY) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) June 2013 © Gwylim Seaton Blackburn, 2013 Abstract I investigated two topics in evolution. The first concerns the potential role of sexual selection in population divergence of H. americanus jumping spiders. Field observations suggest males seldom feed yet travel widely, apparently seeking mates. Males displayed vigorously to females, whereas females appeared highly choosy. The apparent absence of antagonistic ehavior during male-male interactions suggests mate competition in this species is mediated by female choice. I assessed if female preferences for local males promote reproductive isolation among three H. americanus populations that are each monomorphic for a different male sexual display morph. Supporting this idea, virgin females copulated more often with local compared to foreign males during mate trials. However, the effect of other mating interaction components on mating success remains to be resolved. All crosses produced offspring, ruling out strong intrinsic reproductive barriers among morphs and suggesting divergent female mate preferences may constitute an early source of reproductive isolation. I documented low genetic divergence among several populations, further indicating selection underlies the stark display differences between them. Further, this force appears to counteract gene flow: among-morph population comparisons show “isolation by distance”, despite the fact that phenotypically similar populations, which are scattered widely across the study area, are relatively closely related. This implies a greater exchange of genes between phenotypically similar populations. Collectively, these results implicate divergent selection on, or correlated with, male sexual displays at an early stage of differentiation in this species. In a separate study, two colleagues and I use genetic models to demonstrate that sex ratio adjustment (SRA) by parents can reduce intralocus sexual conflict (IASC) by directing alleles of a sexually antagonistic trait to the sex of offspring they benefit. If the trait is autosomally inherited, this strategy evolves irrespective of which parent’s genotype SRA is based on. It can also evolve when the trait is sex-linked, provided decisions are based on the genotype of the homogametic sex—SRA based on the heterogametic sex instead promotes fixation of the allele that is detrimental to that sex. These results suggest sexual conflict might account for previously unexplained variation in the occurrence of SRA in nature. ii Preface A version of Chapter 5 has been published as: “Blackburn, G.S.B., Albert, A.Y.K., and Otto, S.P. (2010). The evolution of sex ratio adjustment in the presence of sexually antagonistic selection. The American Naturalist (176) 3, 264-275”. I generated the original idea for the project and developed the final scope of the study with Sally Otto. I built recursion equations for the analytical models. Arianne Albert and Sally isolated model conditions that favor the evolution of sex ratio adjustment (SRA). Sally designed a simulation for the long-term evolution of SRA. I modified the simulation for alternative genetic architectures and Sally and I compiled simulation results. Sally wrote or strongly guided my writing of the Results, and she also created the article figures. I wrote most of the remaining manuscript. The behavioral experiment in Chapter 3 was approved by the UBC animal care committee (A06-1540). Permits for spider collection were obtained from the Yosemite National Park (YOSE 2007 SCI 0045, YOSE 2010 SCI 0068). iii Table of contents Abstract ............................................................................................................................... ii Preface ................................................................................................................................ iii Table of contents ................................................................................................................ iv List of tables ...................................................................................................................... vii List of figures ................................................................................................................... viii Acknowledgements ............................................................................................................. x Dedication ......................................................................................................................... xii Chapter 1: Introduction .......................................................................................................... 1 1.1 Sexual selection and speciation .......................................................................... 1 1.1.1 Trends in the study of sexual selection with respect to speciation ................. 2 1.1.2 Study system: Habronattus jumping spiders (Aranae, Salticidae) ................. 5 1.1.3 Research goals ................................................................................................ 6 1.2 Sex ratio adjustment in the presence of sexually antagonistic selection ............ 7 1.2.1 Trends in the study of intralocus sexual conflict and sex allocation .............. 7 1.2.2 Research goals ................................................................................................ 9 Chapter 2: Characterizing sexual selection from natural breeding ehavior in two species of jumping spider, Habronattus americanus and H. ophrys .............................................. 10 2.1 Summary ........................................................................................................... 10 2.2 Introduction....................................................................................................... 10 2.3 Methods ............................................................................................................ 13 2.4 Results .............................................................................................................. 14 2.4.1 Factors affecting mate search effort ............................................................. 15 2.4.1.1 Travel .................................................................................................. 15 2.4.1.2 Feeding and hunting ............................................................................ 15 2.4.2 Behavioral interactions ................................................................................. 16 2.4.2.1 Intersexual encounters ........................................................................ 16 2.4.2.2 Male-male encounters ......................................................................... 17 2.5 Discussion ......................................................................................................... 19 2.5.1 Mate search effort ......................................................................................... 19 2.5.2 Intersexual mate choice ................................................................................ 19 2.5.3 Direct contests among males ........................................................................ 21 2.5.4 Environmental signal conditions during courtship ....................................... 22 2.5.5 Conclusions .................................................................................................. 23 2.6 Acknowledgements........................................................................................... 23 Chapter 3: Divergence in female mate choice and male sexual displays among conspecific jumping spider populations, despite the absence of strong postmating barriers ........... 30 3.1 Summary ........................................................................................................... 30 3.2 Introduction....................................................................................................... 30 3.3 Methods ............................................................................................................ 32 3.3.1 Spider collection and care ............................................................................. 32 3.3.2 Mate trials ..................................................................................................... 33 3.3.3 Predicted patterns of mate choice ................................................................. 34 3.3.4 Fertilization status ......................................................................................... 35 3.3.5 Postzygotic reproductive success ................................................................. 36 3.3.6 Statistical analyses ........................................................................................ 37 3.4 Results .............................................................................................................. 38 iv 3.4.1 Mating success .............................................................................................. 38 3.4.1.1 Copulation occurrence ........................................................................ 38 3.4.1.2 Latency to copulate ............................................................................