The Maintenance of Sperm Variability: Context-Dependent Selection on Sperm Morphology in a Broadcast Spawning Invertebrate

Abstract

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness? A key to understanding the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly context dependent. Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature. We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high-concentration environments, whereas sperm with long heads were favored at low concentrations and old ages. We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males. Some of the most fundamental and enduring questions in evolutionary biology concern the evolution of gamete size and morphology (e.g., Kalmus 1932; Scudo 1967). The evolutionary forces shaping gamete morphology may be nuanced, complex, and are incompletely understood (see reviews by Randerson and Hurst 2001;Snook 2005). There has been a sustained and intense effort by theoreticians to model the evolution of anisogamy (small sperm and large eggs; Parker et al. 1972, Parker 1982Levitan 1993;Dusenbery 2000;Lehtonen and Kokko 2011), but the assumptions underlying these models have received less empirical attention. In particular, although it now seems clear that males that produce more sperm may often secure more fertilizations, the role of sperm quality has been less explored. Indeed, a recent focus on sperm quality has highlighted the importance of understanding the evolutionary forces that shape not only sperm size, but also fertilization performance and its morphological underpinnings (reviewed by Snook 2005).Although formal analyses of selection on sperm morphology are rare, one line of evidence to suggest an adaptive role for sperm morphology is the theoretical link between morphological traits (e.g., size and shape of sperm components) and sperm function, especially swimming speed (reviewed by Humphries et al. 2008).

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

“…We did not conduct trials with sperm competition because we were interested in alternative mechanisms of sperm evolution and lacked the capacity to assign zygote paternity via molecular analyses. Free-spawned eggs in nature are often faced with sperm limitation [11,12], making our trials ecologically relevant to this mating system (see also [39,40]) but nonetheless limited to inferring selection pressures in the absence of competition. Trials were conducted in 13 replicate blocks with 5-11 males per block.…”

Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

“…Nevertheless, sperm phenotype also covaries with the paternal phenotype or paternal environment, and it is this non-genetic variation that is relevant to this review. For example, non-genetic factors such as size, age and condition can vary with sperm morphology in some species but not others (Devigili et al, 2013;Johnson et al, 2013;Pitnick et al, 2008a;Rakitin et al, 1999;Schulte-Hostedde and Millar, 2004). Sperm morphology can also vary in time (Lüpold et al, 2012) and space Manier and Palumbi, 2008;Marks et al, 2008;Schmoll and Kleven, 2011).…”

“…More recently, however, there has been growing evidence that selection on sperm phenotype is context dependent, such that different phenotypes will be favoured under different conditions (Crean and Marshall, 2008;Fitzpatrick et al, 2007). For example, Johnson et al (Johnson et al, 2013) showed that when sperm were able to access eggs immediately, sperm with long tails and smaller heads were favoured, but when sperm accessed eggs after ageing, sperm with larger heads were favoured. Differential selection on sperm phenotypes under different conditions has, in some species at least, led to the evolution of gamete plasticity whereby males adaptively adjust the phenotype of their sperm in accordance with their local environment.…”

“…Accordingly, a number of studies have shown that males adjust the phenotype of their sperm in response to their perceived risk of sperm competition. For example, males alter the phenotype of their sperm according to mating mode, social status and the density of other males in groups as diverse as fish, chickens, ascidians, annelids and humans (Crean and Marshall, 2008;Fitzpatrick et al, 2007;Immler et al, 2010;Johnson et al, 2013). Crean and Marshall (Crean and Marshall, 2008) showed that males alter the phenotype of their gametes in response to increases in the risk of sperm competition, and that this gamete plasticity resulted in higher fertilisation success when sperm concentrations were high.…”

Sperm chemotaxis promotes individual fertilization success in sea urchins

“…In particular, gamete characteristics operating at the scale of a single cell have been shown to mediate population-and individual-level differences in reproduction Snook, 2005;Fitzpatrick et al, 2012;Fitzpatrick and Lüpold, 2014;Simpson et al, 2014;Levitan, 2000;van der Horst and Maree, 2014). Sea urchin males with faster sperm have greater fertilization success (Levitan, 2000) and, in low sperm concentration situations, marine tube worm sperm head length correlates with relative fitness (Johnson et al, 2013). Gamete recognition factors are also known to play a role in sperm competition and fertilization success (Swanson and Vacquier, 2002;Palumbi, 1999;Zigler et al, 2005).…”