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Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila?

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Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila? Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila? by Tiffini Smith B.A. in Biological Sciences, December 2012, Virginia Commonwealth University A Thesis submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Master of Science May 20, 2018 Thesis directed by Mollie Manier Assistant Professor of Biology ã Copyright 2018 by Tiffini Smith All rights reserved Dedication I want to dedicate this thesis to the family and friends that have supported me throughout this journey. I would also like to dedicate this thesis to all the first, only, and different people in the world that are breaking barriers, following their dreams, and paving the way for those like them. iii Acknowledgements I wish to acknowledge my fellow graduate students specifically the students in Dr. Patricia Hernandez and Dr. Arnaud Martin lab for answering questions, providing support, and being sounding boards for my projects. iv Abstract of Thesis Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila? In polyandrous species, the sperm of multiple males may coexist within the female reproductive tract, generating postcopulatory sexual selection (PCSS) that can lead to rapid diversification of male and female traits. In Drosophila, PCSS drives the evolution of extremely long sperm, which are also coevolving with the female sperm storage organ, the seminal receptacle (SR). This male-female coevolutionary dynamic may be mediated by Fisherian sexual selection, fueled by a genetic correlation between SR length and sperm length. SR length is also genetically correlated with remating rate within D. melanogaster, suggesting that the intensity of PCSS may be driving the evolution of SR length in this species. Here, I ask if this microevolutionary process can explain the macroevolutionary pattern of male-female coevolution across the Drosophila lineage. I investigate the association between PCSS and SR length across 17 Drosophila species and find that they are not significantly associated. I additionally test alternative hypotheses that SR evolution is mediated by natural selection on fecundity and again fail to find support for this hypothesis. Although it is assumed that Fisherian sexual selection drives the evolution of extraordinarily long sperm through postcopulatory female choice mediated by SR length, it is still unclear what is driving SR evolution v Table of Contents Dedication .......................................................................................................................... iii Acknowledgements ............................................................................................................ iv Abstract of Thesis ............................................................................................................... v List of Figures ................................................................................................................... vii List of Tables ................................................................................................................... viii List of Symbols / Nomenclature ........................................................................................ ix Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila?......................................................................................................................... 1 Methods............................................................................................................................... 9 Results ............................................................................................................................... 12 Discussion ......................................................................................................................... 13 Conclusions ....................................................................................................................... 15 References ......................................................................................................................... 16 Figure Legend ................................................................................................................... 26 Figures............................................................................................................................... 27 Table Legend .................................................................................................................... 31 Tables ................................................................................................................................ 32 List of Figures Figure 1 ............................................................................................................................. 27 Figure 2 ............................................................................................................................. 27 Figure 3 ............................................................................................................................. 28 Figure 4 ............................................................................................................................. 28 Figure 5 ............................................................................................................................. 29 Figure 6 ............................................................................................................................. 29 Figure 7 ............................................................................................................................. 30 vii List of Tables Table 1 .............................................................................................................................. 32 Table 2 .............................................................................................................................. 33 Table 3 .............................................................................................................................. 34 viii List of Symbols / Nomenclature 1. PCSS: Postcopulatory Sexual Selection 2. CFC: Cryptic Female Choice 3. FRT: Female reproductive tract 4. SR: Seminal Receptacle 5. SSO/SSOs: Sperm storage organ/s 6. PIC: Phylogenetic Independent Contrast ix Does Sexual Selection Drive the Evolution of the Female Sperm Storage Organ in Drosophila? In polyandrous species, the sperm of multiple males may coexist within the female reproductive tract, generating postcopulatory sexual selection (PCSS) in the form of sperm competition (Parker 1970) or cryptic female choice (Eberhard 1996) that may bias sperm use for fertilization. Male adaptations to PCSS in sperm include increased swimming speed and energetics, as well as modified sperm morphology to compete for position, storage, and ultimately fertilization (Parker 1970; Birkhead et al., 1999; Hunter & Birkhead 2002; Higginson et al., 2012; Arnqvist 2014; Firman et al., 2017). It is not enough for sperm to be fertilization competent; sperm must successfully fertilize eggs in sperm competition to have reproductive success. Sperm competition as a Mechanism of PCSS Sperm competition is male-male competition that in internal fertilizers occurs within the female reproductive tract (FRT), where successful sperm have a greater fertilization rate and increase the reproductive success of the respective male. This competition causes male traits to experience a high degree of diversification and evolution; this rapid evolution provides an avenue for males to adapt to better compete in sperm competition to enhance paternity success (Miller & Pitnick 2002; Manier et al., 2013c). Sperm has been shown to develop adaptations in swimming speed, sperm energetics (energy due to ATP content which enhances sperm swimming), as well as sperm morphology to compete for position, storage and ultimately egg fertilization (Miller & Pitnick 2002; Lüpold et al., 2009; Higginson et al., 2012; Manier et al., 2013c; Rowe et al., 1 2013; Fitzpatrick & Lüpold 2014; Rowe et al., 2015). Rowe et al., (2015), showed in passerine birds that sperm competition drives the evolution of midpiece and flagellum length which is positively correlated with swimming speed (Rowe et al., 2015) and is hypothesized to increase thrust and aid drag resistance during sperm competition (Lüpold et al., 2009; Rowe et al., 2015). Postcopulatory sexual selection can also drive the evolution of sperm length. Miller and Pitnick (2002) used Drosophila melanogaster to demonstrate that long sperm outcompete short sperm during sperm competition. The caveat being that long sperm only outcompete short sperm in long seminal receptacles (sperm storage organ; Miller & Pitnick 2002). This indicates reproductive success is not solely mediated by the male. Cryptic Female Choice as a Mechanism of PCSS Females can also alter reproductive success of males by using cryptic female choice (CFC) to control and bias sperm. Cryptic female choice (Thornhill 1983), the second major mechanism of PCSS, is generally defined as the use of morphological, biological, and behavioral mechanisms by polyandrous females to create nonrandom paternity biases (Pitnick & Brown 2000). Females can bias paternity at any stage of the reproductive process, including through control of copulation duration, sperm ejection, sperm storage, and sperm use for fertilization (Birkhead & Møller 1993; Pitnick
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