Sperm morphometry (i.e., size and shape) is thought to be closely associated with sperm function and therefore male fertilization success and fitness (Birkhead and Pizzari 2002; Pizzari and Birkhead 2002). The association between sperm function and morphometry, including the size of the head, midpiece, and flagellum, is empirically supported across different species (Fitzpatrick et al. 2009; Lüpold et al. 2009), and also within species (Gage et al. 2004; Birkhead et al. 2005; Humphries et al. 2008; Mossman et al. 2009). It seems plausible that intraspecific variation in sperm morphometry causes variation in sperm function, and hence variation in fertilization success and male fitness. Postcopulatory sexual selection and sperm competition in particular is thought to exert selection pressure on sperm function and morphometry stabilizing around an optimal sperm design (Parker 1998; Pizzari and Birkhead 2002; Calhim et al. 2007; Immler et al. 2008). In fact, increased selection due to increased risk of sperm competition has been shown to reduce intraspecific variation in sperm morphometry (Calhim et al. 2007). Despite this, variation at the intraspecific level persists and may be an important determinant of relative reproductive fitness among males.
Several studies have found sperm morphometry to be highly heritable (Woolley and Beatty 1967; Morrow and Gage 2001a; Simmons and Kotiaho 2002; Birkhead et al. 2005) and sperm morphometry is known to exhibit little variation within males (Morrow and Gage 2001b; Immler et al. 2008). However, two recent studies indicate that sperm morphometry can also be—at least to some extent—a phenotypically plastic trait (Crean and Marshall 2008; Morrow et al. 2008), which may be adjusted to population density (and hence intensity of sperm competition; Crean and Marshall 2008). Given that the intensity of sperm competition may vary between males within a species (Parker 1990), and that males alter other ejaculate traits, such as sperm number and sperm motility (Pilastro et al. 2002; Cornwallis and Birkhead 2007), according to varying social conditions, it seems plausible that at least some of the intraspecific variation in sperm morphometry may relate to male quality or strategic investment.
Dominant and subordinate males often use different mating strategies, which may have a pronounced effect on their physiology, including stress (corticosterone) and sex hormone levels (testosterone; Husak and Moore 2008). These hormones are also known to strongly influence ejaculate traits, often with contrasting effects. For example, testosterone is vital for sperm production (Maddocks and Setchell 1988; Jones and Lin 1993; Kast et al. 1998), whereas corticosterone may inhibit the production of sperm (Wingfield and Sapolsky 2003). However, it is unclear how these differences in hormone levels between dominant and subordinate males influence the strategic investment in ejaculate traits, such as sperm number (Gage et al. 1995; Neff et al. 2003; Pizzari et al. 2003) and sperm velocity (Burness et al. 2004; Cornwallis and Birkhead 2007). Furthermore, it is unknown whether changes in the social environment and resulting changes in hormone levels have any impact on sperm morphometry and/or function and also whether males are able to adjust sperm morphometry to different conditions and situations. In the bluegill sunfish (Lepomis macrochirus), for example, dominant (i.e., territorial) and subordinate (i.e., sneaker) males differ in sperm length (Burness et al. 2004), but whether this difference exists due to adjustment by the males to given conditions or whether this is correlated with other traits relating to male reproductive strategy is unknown.
Here we experimentally evaluate within-individual plasticity (i.e., relative changes before vs. after the experiment for the same males) in sperm morphometry in varying social contexts, and the associated changes in aggression and stress hormones in the color polymorphic Gouldian finch (Erythrura gouldiae). Head color in this socially monogamous bird is genetically determined and related to distinctive dominance behaviors: red males are dominant over black males and overtly aggressive, whereas black males are submissive to red males (Pryke and Griffith 2006). These different competitive strategies between morphs are tightly linked to the divergent production of aggression (testosterone) and stress (corticosterone) hormones (Pryke et al. 2007). Red males are highly reactive to changes in the social environment, especially towards the relative densities of their own morph, displaying elevated aggression (testosterone) and stress (corticosterone) responses in socially competitive environments (Pryke et al. 2007). In contrast, the nonaggressive black males follow a more passive strategy, where aggression and stress hormone levels are largely unaffected by the relative competitive environment (Pryke et al. 2007). We took advantage of these behavioral differences between the morphs to create environments with varying social competition to test potential effects on sperm morphometry and function.