Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

Abstract

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory—broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal. Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae). We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size. Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

Sperm duct gland contents increase sperm velocity in the sand goby

“…As females often take hours to deposit their eggs, this dual mode of sperm release likely reduces the male trade-off between fertilization and nest-guarding against sneaker males (Marconato et al, 1996; Scaggiante et al, 1999). In addition, a slow release of small ejaculates has been linked to increased fertilization success in an externally fertilizing polychaete and this may apply to fish as well (Olito and Marshall, 2018). Sperm of externally spawning fishes typically have a short functional life, that in most cases is limited to minutes or even seconds (Cosson et al, 2008).…”

Density‐dependent patterns of multivariate selection on sperm motility and morphology in a broadcast spawning mussel

“…In broadcast spawners, mating, and fertilization success is determined by gamete interactions, with little to no opportunity for adults to control their mating partners (Evans & Lymbery, 2020). Additionally, gamete interactions and fertilization success for broadcast spawners are impacted by the density and sex ratio of individuals participating in a spawning event (Levitan, 2004, 2005; Levitan & Ferrell, 2006; Pennington, 1985; Yund, 2000), water turbulence and flow (Crimaldi, 2012; Denny & Shibata, 1989; Levitan, 2018), and the timing and rate of gamete release (Benzie & Dixon, 1994; Marshall & Bolton, 2007; Olito & Marshall, 2019). As a result, local sperm densities (i.e., within the “capture zone” of individual ova; Levitan, 2018) range from conditions that result in sperm limitation, when there are too few sperm to fertilize all available eggs, to sperm saturation, where an excess of sperm heightens the risk of polyspermy (multiple sperm fertilizing a single egg), leading to embryonic failure (Levitan, 1998; Styan, 1998; Yund, 2000).…”