The Adaptive Function of Male Genital Spines in the Fruit Fly Drosophila Ananassae [Doleschall] (Diptera: Drosophilidae)

The adaptive function of male genital spines in the fruit fly Drosophila ananassae [Doleschall] (Diptera: Drosophilidae) A thesis submitted to the Division of Research and Advanced Studies of the University of Cincinnati In partial fulfillment of the requirements for the degree of MASTER OF SCIENCE In the Department of Biological Sciences of the McMicken College of Arts and Sciences 9 July 2012 by Karl Grieshop B.S., University of Cincinnati June 2009 Committee Chair: Dr. Michal Polak 1 ABSTRACT Chapter 1: That male genital morphology evolves via postcopulatory sexual selection is a widely held view. In contrast, the precopulatory sexual selection hypothesis for genital evolution has received less attention. Here, we test the hypothesis that male genital spines of Drosophila ananassae promote competitive male copulation success. Using laser surgery to manipulate trait size, we demonstrate that incremental reductions of spine length progressively reduce male copulation success: males without spines failed entirely to copulate because of an inability to couple the genitalia together, whereas males with halfway ablated and blunted spines suffered reductions in copulation success of 87% and 13%, respectively. The decrease in copulation success resulting from spine length reduction was markedly stronger in sexually competitive environments than in non-competitive environments, and females expressed resistance behaviors similarly toward competing male treatments, demonstrating directly the role of genital spines in promoting competitive copulation success. Because these spines are widespread within Drosophila, and because genital traits with precopulatory function are being discovered in a growing number of animal taxa, precopulatory sexual selection may have a more pervasive role in genital evolution than previously recognized. Chapter 2: The contemporary explanation for the rapid evolutionary diversification of animal genitalia is that such traits evolve via postcopulatory sexual selection. The most common debate within this framework has been over the relative importance of three non-mutually exclusive evolutionary mechanisms: sperm competition, cryptic female choice, and sexual conflict. The first two of these are strictly postcopulatory mechanisms, whereas sexual conflict could operate before, during or after copulation. We investigate the potential for male genital spines in Drosophila ananassae to function in postcopulatory sexual selection. Whereas previous work on two Drosophila species shows that these spines function in precopulatory sexual selection to promote male competitive copulation success, the postcopulatory function(s) of Drosophila genital spines have not yet been thoroughly investigated. Using a precision micron-scale laser surgery technique we test the effect of spine length reduction on male competitive fertilization success, female remating behavior, fecundity, and copulation duration. We find no evidence that male genital spines in this species have a postcopulatory adaptive function. However, partial genital spine ablation had an unexpected positive effect on the probability that males would fertilize at least one gamete of a previously mated female. This effect is discussed in terms of the possibility that Drosophila genital spines are harmful to females as a pleiotropic side effect of evolving to promote competitive male copulation success. 2 COPYRIGHT NOTICE Regarding Chapter 1, published in Evolution (The International Journal of Organic Evolution): AUTHORS - If you wish to reuse your own article (or an amended version of it) in a new publication of which you are the author, editor or co-editor, prior permission is not required (with the usual acknowledgements). However, a formal grant of license can be downloaded free of charge from Rightslink if required. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1558-5646/homepage/Permissions.html 3 GENERAL INTRODUCTION Evolutionary biologist are interested in traits that vary across closely related taxa, because this indicates that such traits have undergone some type of rapid divergent evolution relative to the traits that do not vary across those taxa. The most famous example of this is the disparate beak morphologies exhibited by finches of the Galapagos Islands, which aided Charles Darwin’s formulation of the modern theory of evolution (Darwin, 1859). Darwin identified these various beak morphologies as being adaptive within particular evolutionary lineages because their distinct, specialized functions (e.g. foraging for large seeds versus small seeds) allowed individuals bearing the optimal foraging hardware to out-compete those with more generalized morphological equipment in the life or death competition for survival. He termed this process by which nature provides individuals of a population with differential fitness (defined as survival and reproduction) natural selection, where individuals with relatively greater fitness are better able to pass on the heritable components of their success to their offspring, which in turn share such success. The result, over evolutionary time, is the formation of distinct species that occupy different ecological niches. The most variable type of morphological trait exhibited across even closely related species of the animal kingdom is that of male genitalia (Eberhard, 1985). However, contrary to the beak morphologies of Darwin’s finches that have evolved to exploit specialized niches, male genital traits and their functions are variable across closely related taxa that occupy the same or similar niches. The inference here is that natural selection would not operate on such closely related, similar species in such a variety of ways, whereas sexual selection—a type of natural selection concerned specifically with differential reproductive fitness of individuals (Darwin, 1871)—could account for such a pattern of evolutionary diversification under similar naturally 4 selective pressure(s) (Lloyd, 1979; Eberhard, 1985). Darwin (1871) reserved sexual selection for explaining only the bizarre and elaborate secondary sexual traits of animals (e.g. the peacock’s tail), and evolutionary biologists have only recently begun implicating sexual selection in the evolution of primary sexual traits, such as male genital morphology (Eberhard, 1985; Shapiro & Porter, 1989; Hosken & Stockley, 2004; Leonard & Córdoba-Aguilar, 2010). Since this latest paradigm shift in the understanding of genital trait evolution, most studies of genital traits have focused on a particular type of sexual selection that ensues after the onset of copulation—postcopulatory sexual selection. This is understandable considering most genital traits do not contact the opposite sex until copulation has begun. But lately a growing body of evidence for genital traits functioning prior to copulation has emerged, despite its counterintuitive plausibility (Bertin & Fairbairn, 2005; Langerhans et al., 2005; Kahn et al., 2010; Polak & Rashed, 2010; Miller, 2010). This thesis investigates the adaptive function of a specific genital trait, male genital spines, of the fruit fly Drosophila ananassae. Though insects offer abundant opportunity to study the adaptive function of animal genitalia because they are easily maintained and manipulated in a laboratory, and typically yield high sample sizes, most insect genitalia are microscopic in size—a practical research impediment to the manipulative experimentation that reveals the causal bases, or selective pressures, responsible for the evolution of these traits. To address this dilemma, a novel micron-scale laser ablation technique is used to perform precision surgeries, generating discrete experimental treatments that can be used to answer specific questions regarding the function of male genital spines in this species. The experiments described in the following two chapters contribute to an underrepresented area of the literature: the role of precopulatory sexual selection in the evolution of genital trait form and function. 5 REFERENCES Darwin, C. 1859. On the origin of species by means of natural selection. London, UK: John Murray. Darwin, C. 1871. The descent of man, and selection in relation to sex. London, UK: John Murray. Eberhard, W. G. 1985. Sexual selection and animal genitalia. Cambridge, MA: Harvard University Press. Hosken, D. J. & Stockley, P. 2004. Sexual selection and genital evolution. Trends Ecol. Evol. 19:87-93. Kahn, A. T., Mautz, B., & Jennions, M. D. 2010. Females prefer to associate with males with longer intromittent organs in mosquitofish. Biol. Letters. 6:55-58. Langerhans, R. B., Layman, C. A., & DeWitt, T. J. 2005. Mal genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proc. Natl. Acad. Sci. USA. 102:7618-7623. Leonard, J. L. & Córdoba-Aguilar, A. (eds) 2010. The evolution of primary sexual characters in animals. New York, NY: Oxford University Press. Lloyd, J. E. 1979. Mating behavior and natural selection. Fla. Entomol. 62: 17-34. Miller, E. H. 2010. Genitalic traits of Mammals. In: The evolution of primary sexual characters in animals (J. L. Leonard, A. Córdoba-Aguilar, eds), pp. 471-493, New York, NY: Oxford University Press. Polak, M. & Rashed, A. 2010. Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc. R. Soc. Lond. B. Biol. Sci. 277:1371-1376. Shapiro, A. M. & Porter, A. H. 1989. The lock-and-key hypothesis: evolutionary and biosystematic interpretation of insect genitalia. Annu.

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