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Abstract Species with alternative reproductive strategies are characterized by discrete differences among males in suites of traits related to competition for fertilizations. Models predict sneaker males should allocate more resources to their ejaculates because they experience sperm competition more frequently and often occupy a disfavoured ‘role’ owing to subordinance in intramale competition and female preferences for larger males. We examined whether sperm number and quality differed between male strategies in the internally fertilized fish Xiphophorus nigrensis and explored the relationship between sperm morphology and performance. We found sneaker males had similar testes sizes compared to courting males but ejaculates with both more viable and longer lived sperm. Sneaker sperm also had longer midpieces, which was positively correlated with both velocity and longevity. Our study suggests that the evolution of sperm quantity and quality can be decoupled and that the sperm morphology is likely to play an important role in mediating sperm competition through its effects on sperm performance.
Sperm competition, or competition between sperm of two or more males for a set of ova, has widespread effects on the evolution of animals (Birkhead & Møller, 1998). Sperm competition’s role in evolution may be particularly prominent in species with alternative reproductive strategies, where suites of physiological, morphological and behavioural traits have diversified among males as a result of competition for fertilizations (Oliveira et al., 2008). Male mating strategies commonly take two forms, a ‘bourgeois’ strategy that attempts to monopolize females or the resources they require to mate and a ‘parasitic’ strategy that exploits the bourgeois strategy by sneaking copulations with the females they attract (Taborsky, 1998). Given a trade-off between investment in ejaculates and other traits necessary for obtaining mates (e.g. courtship, territory defence), models predict parasitic males should allocate more resources to their ejaculates because (i) parasitic males are typically at a disadvantage (occupy a disfavoured ‘role’) in mating because of subordinance in male–male competition and female preferences for bourgeois males (Parker, 1990a) and (ii) parasitic males often have a higher risk of sperm competition, that is they experience sperm competition more frequently than bourgeois males (Parker, 1990b).
A universal expectation of theory is that investment in spermatogenesis should increase with sperm competition risk (Parker, 1998). As predicted, ejaculate sizes are typically larger in parasitic males (Taborsky, 1998). Studies using phylogenetic approaches, experimental evolution and analyses of phenotypic plasticity have found similar responses of traits influencing sperm number. Testes size often increases in species where females mate multiply (Birkhead & Møller, 1998), increases when polyandry is experimentally enforced in evolving populations (Hosken & Ward, 2001; Pitnick et al., 2001; LaMunyon & Ward, 2002; Simmons & García-González, 2008; but see Crudgington et al., 2009), and males facultatively increase their ejaculate size when the perception of sperm competition risk is heightened (Wedell et al., 2002; Pizzari et al., 2003, Rudolfsen et al., 2006, delBarco-Trillo & Ferkin, 2006). A few notable exceptions, however, exist where species with alternative male strategies show no differences in testes or ejaculate size between male morphs (Simmons et al., 1999; Neat, 2001; Byrne, 2004; Kelly, 2008). The discrepancy between theory and data is most commonly ascribed to a violation of the model’s assumptions (Parker, 1990a). For example, if the frequency of the parasitic males in the population is high enough, the risk of sperm competition might be equivalent for each tactic, resulting in no difference in ejaculate investment.
In addition to variation in the number of sperm available for mating, sperm competition may affect the quality of the sperm males produce. Sperm size, for example, has been hypothesized to increase fertilization success by increasing longevity, swimming speed, or ability to displace rival males’ sperm and varies markedly within and among species (Pitnick, 1996; Gage, 1998; Ward, 1998; Snook, 2005; Malo et al., 2006; Sherman et al., 2008). Sperm size, however, covaries inconsistently with sperm competition risk among species (Gomendio & Roldan, 1991; Snook, 2005; Fitzpatrick et al., 2009, Lüpold et al., 2009). The lack of a consistent relationship between the theory and data is likely because of differences in the metric chosen to quantify sperm competition risk among studies (Snook, 2005), violations of the assumed relationships between sperm size, swimming speed and longevity (Parker, 1998; Snook, 2005; Humphries et al., 2008) or effects of male–female coevolution on gamete morphology rather than sperm competition risk per se (Eberhard, 1996; Snook, 2005).
Species with alternative reproductive strategies are an important foil for the comparative method because confounds such as differences in female anatomy between species are controlled, and fertilization success between males that differ in ejaculate characteristics can be measured experimentally. In the few species with alternative reproductive strategies that have been examined, sperm size typically does not differ between tactics (Gage et al., 1995; Hettyey & Roberts, 2006; Stoltz & Neff, 2006; Fitzpatrick et al., 2007; Locatello et al., 2007; but see Burness et al., 2004, Simmons et al., 1999). Parasitic sperm, however, have been found to be of higher quality when metrics of sperm performance rather than morphology alone are considered (Vladic & Jarvi, 2001; Locatello et al., 2007). Parasitic male Alantic salmon (Salmo salar), for example, have higher sperm motility, velocity, ATP concentration and sire more offspring when mixed with an equal number of bourgeois sperm (Vladic & Jarvi, 2001). Similarly, parasitic male bluegill sunfish (Lepomis macrochirus) have faster sperm, higher concentrations of ATP (Burness et al., 2004; but see Stoltz & Neff, 2006), and sire twice as many offspring in vitro when differences between males in sperm number are statistically controlled (Stoltz & Neff, 2006). Finally, sperm quality and number covary with tactic in species where male tactic depends on social status. Experimental manipulations of social status in some species have shown that subordinate males (i.e. the disfavoured role) produce more, higher quality sperm compared to their dominant counterparts (Rudolfsen et al., 2006; Cornwallis & Birkhead, 2007, Pizzari et al., 2007; but see Fitzpatrick et al., 2008; Montrose et al., 2008; Kruczek & Styrna, 2009; Thomas & Simmons, 2009).
Information gained from these systems is invaluable because they provide a unique data set for comparison to studies using the comparative method and experimental evolution. Although studies of species with alternative reproductive strategies and external fertilization have produced substantial insights into the role of sperm competition in evolution, species with alternative reproductive strategies and internal fertilization have been less well characterized. Interactions between the sexes and the physical environment in which sperm compete are vastly different between internal and external reproductive modes, and as a consequence we might expect the selective forces on ejaculate traits to also differ. In external fertilizers, sperm swimming speed rather than longevity is thought to be optimized in response to sperm competition, because reproductive success is dependent on sperm–egg collision rate over a short period of time (Parker, 1993). In contrast, mating and fertilization are often decoupled in internal fertilizers, particularly in those species with sperm storage. As a consequence, traits that increase sperm survival (Taborsky, 1998; Birkhead et al., 1999; Pizzari et al., 2008) or facilitate the displacement of rival sperm within the female reproductive tract, such as sperm size (LaMunyon & Ward, 1998), may confer a selective advantage.
In this study, we characterize variation in sperm quantity and quality between alternative reproductive strategies in the internally fertilized swordtail Xiphophorus nigrensis. Regardless of reproductive mode, the canonical expectation is that investment in sperm number should be greater for males that face either a higher risk of sperm competition or occupy a disfavoured ‘role’ in mating (Parker, 1990a,b), and as a consequence we expect investment in spermatogenesis should be greater for parasitic males (Taborsky, 1998). How sperm quality should vary with sperm competition risk, however, is less well understood, and model expectations depend on the assumed relationships between sperm size, velocity and longevity (Parker, 1993). Models clearly predict larger, faster sperm should evolve with increased sperm competition risk at the expense of longevity when reproductive success is determined by a race to the egg (c.f. external fertilization, Parker, 1993). If reproductive success is primarily mediated by surviving a period of sperm storage, however, sperm survival (and sperm size) only varies with risk if more strict assumptions are met; for example, if the evolution of sperm number is constrained or the benefits of sperm size increase with sperm density in competition (Parker, 1993). Although many studies have considered the relationship between sperm size and risk, debate continues over the expected relationships between morphology and performance (Malo et al., 2006, Humphries et al., 2008) central to model predictions. Here, we also examine the covariation between sperm morphology and performance in the context of the evolution of alternative reproductive strategies.