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The ecology and evolution of female-specific ornamentation in the dance flies (Diptera: Empidinae) Rosalind L. Murray Doctor of Philosophy, 2015 Biological & Environmental Sciences University of Stirling © Copyright by Rosalind L. Murray 2015 The ecology and evolution of female-specific ornamentation in the dance flies (Diptera: Empidinae) Rosalind L. Murray Abstract Elaborate morphological ornaments can evolve if they increase the reproductive success of the bearer during competition for mates. However, ornament evolution is incredibly rare in females, and the type and intensity of selection required to develop female-specific ornamentation is poorly understood. The main goals of my thesis are to clarify the relationship between the type and intensity of sexual selection that drives the evolution of female ornamentation, and investigate alternative hypotheses that might be limiting or contributing to the development of female ornaments. I investigated the ecology and evolution of female-specific ornaments within and between species of dance flies from the subfamily Empidinae (Diptera: Empididae). The dance flies display incredible mating system diversity including those with elaborate female-specific ornaments, lek-like mating swarms, aerial copulation and nuptial gift giving. To elucidate the form of sexual selection involved in female-ornament evolution, I experimentally investigated the role of sexual conflict in the evolution of multiple female- specific ornaments in the species Rhamphomyia longicauda. Through manipulative field experiments, I found that variation in the attractiveness of two ornaments displayed by females indicates that sexual conflict, causing a coevolutionary arms race, is an important ii force in the evolution of multiple extravagant female ornaments. Using R. longicauda again, I tested for a role of functional load-lifting constraints on the aerial mating ability of males who paired with females displaying multiple large ornaments. I found no evidence of functional constraints influencing the mating opportunities of elaborately ornate females, but instead discovered a relationship consistent with positive assortative mating for mass. Biased sex ratios are predicted to increase the intensity of sexual selection in a population, which in turn, is predicted to influence the evolution of ornamentation. I measured the incidence and prevalence of vertically transmitted symbiotic bacteria that has been observed to distort the sex ratio in other Dipteran hosts. While my survey revealed that symbionts occur at high incidence and variable prevalence across dance fly hosts, I found no effect of symbiont infection levels on population sex ratios, or female- specific ornament evolution. Further investigation into the relationship between sex ratios and female-ornament evolution using the comparative method revealed that the operational sex ratio (OSR) of a population did not predict continuous measures of female ornamentation across species. However, female-ornament evolution did predict male relative testis investment across species indicating that female ornaments likely indicate increased levels of polyandry. My thesis reveals that sexual selection theory developed to describe male-specific ornament evolution cannot readily be translated to apply to females. I show that male mate choice, rather than functional constraints or ecological associations with bacteria, is likely driving the evolution of female-specific ornaments. I also identify sexual conflict as an important selective force in the evolution of female-specific ornaments. iii Acknowledgements First I would like to thank Luc Bussière for his supervision, encouragement and unyielding patience, and for always having his office door open to visitors with questions. This thesis has also benefited from the advice and guidance of my second supervisor Matt Tinsley. Thanks to Prof. Phyllis Lee and Prof. Karim Vahed for serving as my viva examiners. Adrian Plant supplied invaluable feedback and assistance with fieldwork and sample identification. Lilly Herridge offered constant (and patient) field and statistical support and advice. Rob Ness, Lilly Herridge and Tom Houslay provided invaluable feedback at various stages during the writing of this thesis. I collected specimens for this work from the Scottish Centre for Ecology and the Natural Environment (SCENE) at Loch Lomond, Scotland and the “Gwynne Field Station” near the Gwynne family home outside Toronto, Ontario, Canada. I felt very welcomed at both of my field sites, but I would like in particular to thank Rhiannon, Sarah and Darryl Gwynne for their hospitality, warmth and support during my 2012 field season. I would also like to thank Jill Wheeler for introducing me to the R. longicauda field site. The Gwynne lab at the University of Toronto Mississauga were incredibly welcoming and provided insight, guidance and discussion whenever necessary during my stay in Toronto. My sister, Olivia, provided impressive (if unexpected) motivation for my 2012 field season, as well as emergency freezer space and assistance in dance fly model construction. I would like in particular to thank my niece, Lydia, without whom I might never have gone to Ontario to study R. longicauda. Thank-you also to Lydia for waiting until after the flies had left for the season before arriving. I have made many friends that have made my time at Stirling most enjoyable: Lilly Herridge and Tom Houslay for their help and guidance and for being excellent tea- drinking, science-thinking lab mates and willing partners in the practice of procrastination; the past and present members of office 3B156, particularly Jen Sjolund, Lilly Herridge, Gill iv Flynt, Romuald “Rab” Rouger, and Paul Lintott for providing never-ending encouragement and coffee; and especially the Bussière Lab for their friendship and discussions (science- related and otherwise) they have offered. I have spent several weeks during my PhD working at the University of Edinburgh. I would like to thank everyone at the Institute of Evolutionary Biology for welcoming me in their offices, labs and coffee room. In particular, I would like to thank Tom Little, the Little Lab, including Phil Wilson, for microscope space; Nick Colegrave and Josephine Pemberton for providing access and office space; the various office mates in 1.54 for putting up with an occasional interloper; Amy Pedersen for advice, support and productive writing retreats; Rob Ness, Peter Keightley and Nick Colegrave for lab space and advice; Laura Ross for statistical advice and encouragement; the IEEG lab group, including Pedro Vale, Darren Obbard and Laura Ross for welcoming me and offering support and advice on early versions of talks. Thanks to Rob Ness for his supper-making, companionship and unending support (both at home and in the lab) and to Lewis, my son, for his constant enthusiasm and daily dose of reality. Thank-you also to my family in Canada, especially my dad, who offered unconditional support and academic encouragement. Finally, thanks to ‘Genes’ who is set to arrive following the completion of this degree but whose inevitable arrival provided an extraordinary amount of motivation for a timely thesis completion. v Table of contents Abstract ....................................................................................................................... ii! Acknowledgements .................................................................................................... iv! Table of contents ........................................................................................................ vi! List of tables ............................................................................................................... ix! List of figures .............................................................................................................. x! Chapter 1 General introduction ................................................................................ 1! Sexual selection theory ....................................................................................................... 1! Female ornamentation ........................................................................................................ 4! The study system ................................................................................................................ 6! Dance fly biology ............................................................................................................. 6! The long-tailed dance fly, Rhamphomyia longicauda ...................................................... 8! Research objectives .......................................................................................................... 11! Chapter 2 The role of sexual conflict in the evolution of multiple sex-specific female ornaments ..................................................................................................... 14! Abstract ............................................................................................................................. 14! Introduction ....................................................................................................................... 15! Methods ............................................................................................................................ 19! Study system ................................................................................................................. 19! Female silhouette creation ...........................................................................................
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