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Strategic Sperm Allocation, Sperm Competition, and an Epigenetically-Based Resolution of the Lek Paradox
AuthorBonilla, Melvin M.
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Anisogamy is what fundamentally defines the sexes. This sexual dimorphism between individuals that produce relatively few large, costly eggs and those that produce large quantities of small, cheap sperm led to the traditional view that females best safeguard their reproductive investment by being monogamous and highly discriminating in their choice of mate. By contrast, because they produce many small, cheap sperm, males are not limited by gamete production, and can maximize their reproductive success by engaging in promiscuity and mating with as many females as possible. Studies involving behavioral observations supported this view, with apparent monandry reported in many taxa. However, the recent molecular revolution has led to the discovery that mixed paternity and hence polyandry are the rule rather than the exception. In addition, it has been well established that females across a wide array of taxa actively engage in polyandry, often in a very discrete manner. It therefore follows that sexual selection is not restricted to the mating stage but continues in the reproductive tract of females. With the discovery of the importance of sexual selection at the post-copulatory stage has come the recognition that, in essence, males compete not for females but rather for eggs, and that females choose sperm rather than males.Because the energetic costs of sperm have been viewed as negligible, compared to the costs and mortality risks associated with male-male competition, courtship and mate searching, sperm competition theory predicts that sperm allocation to females should increase as sperm competition intensifies. However, males rarely, if ever, transmit a single sperm cell to their mates. Instead, males deliver hundreds, thousands, or even millions of sperm in each ejaculate. Ejaculate cost is therefore orders of magnitudes greater than that of a single sperm, and this cost can have profound implications for male reproductive strategies. If ejaculates are indeed costly, males should adaptively allocate sperm in response to the risk of sperm competition and the mating status and reproductive value of their mates. Here, I exploit the unique reproductive characteristics of the pseudoscorpion, Cordylochernes scorpioides, in which males transfer sperm indirectly via a spermatophore deposited on the substrate, as a model system for investigating the consequences of post-copulatory sexual selection for male reproductive strategies.In Chapter 1, I present the results of an experiment designed to test whether males differentially allocate sperm based on female mating status. In this study, virgin males were paired with females that varied in their mating status (ranging from virgin females to females previously paired with up to three males). External spermatophore deposition allowed for the evaluation of sperm allocation in response to female contact with previous males. The study revealed that males discern cues that enable them to assess a female's mating status and bias sperm allocation in favor of virgin females. While the indirect method of sperm transfer by C. scorpioides males allows for a high level of female deceit and control, females of many species are able to influence the number and fate of sperm transferred and are likely to conceal their lack of sexual receptivity to minimize male retaliation. If males cannot accurately assess female receptivity, increased risk of sperm rejection by mated females could outweigh the risk of sperm competition and favor greater sperm allocation to virgin females. This pattern is not accounted for by standard sperm competition models that rarely consider female behavior. Instead, preferential sperm allocation to virgin females seems to be best explained by a significant risk of males wasting ejaculate on mated females that often feign sexual receptivity.In Chapter 2, I investigate whether male ejaculate characteristics are good predictors of reproductive success in a competitive context. When females mate with more than one male, sperm from rival males compete to fertilize ova, and relative number of sperm transferred to the female may frequently be an important determinant of a male's fertilization success. Characterization of male ejaculates across a large, laboratory population of C. scorpioides, in terms of both sperm viability and total sperm number per spermatophore, allowed assessment of these traits in a competitive context. I present results that demonstrate that ejaculate quality is a good predictor of a male's reproductive success when females are polyandrous, and male-male competition extends to the level of the gamete.Finally, in Chapter 3, I develop an epigenetic model to account for the lek paradox. Female preference should act to erode variation in exaggerated male traits. Such directional selection should remove the benefits of choice, yet female choice persists. This is known as the lek paradox, and, while some resolutions have been proposed, most (if not all) rely on the occurrence of mutations every generation as the source of variation on which females choose. While new genetic variation certainly arises each generation, it is far from clear whether this mutational-based input of genetic variation is sufficient to account for the persistence of female choice. Here, I develop a theoretical framework, centered on epigenetics as an alternative mechanism for the maintenance of variation in fitness traits in males and the persistence of high levels of variation in ejaculate quality. Since the epigenome is much more susceptible to environmental stress than is the genome itself, I argue that environmentally-induced variation in epigenetic gene regulation can generate continual variation in the expression of male fitness traits which then provide females with an honest indicator of ejaculate quality.