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

Abstract

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology

“…overall sperm size; Humphries et al, ). Our findings also add to a growing number of studies that support this prediction (Fitzpatrick, Simmons, & Evans, ; Lymbery et al, ; Monro & Marshall, ). As such, measuring nonlinear selection on multivariate sets of sperm traits is likely to be a necessary (though sometimes complicated) step in assessing selection on sperm morphologies and predicting their adaptation to a changing world.…”

“…For males, fertility relies on the ability of sperm to collide and fuse with eggs; hence, selection has ample scope to target sperm traits that are involved in fertilization (Simmons & Fitzpatrick, ). Indeed, in a range of taxa, various aspects of sperm morphology play important roles in mediating sperm swimming performance (Lüpold, Calhim, Immler, & Birkhead, ; Malo et al, ), and ultimately male fertility (Lymbery, Kennington, & Evans, ; Monro & Marshall, ). For instance, sperm swimming speed is dictated by counteracting forces of thrust produced by the tail versus drag produced by the head and midpiece, which respectively house the nucleus and mitochondria (Humphries, Evans, & Simmons, ).…”

“…This mode of fertilization means that water around eggs can contain sperm from multiple males or only one and that eggs can often go unfertilized due to sperm limitation (Hollows, Johnston, & Marshall, ; Levitan, ; Liao et al, ). Consequently, selection can target gamete phenotypes, including egg size and sperm morphology, that increase fertility through effects on both gamete competition and gamete encounter rates (Liao et al, ; Monro & Marshall, ). We created multiple fertilization environments for Galeolaria by independently manipulating water temperature and viscosity to reflect current‐day conditions, plus progressive levels of near‐term and longer‐term warming.…”

Egg‐induced changes to sperm phenotypes shape patterns of multivariate selection on ejaculates

“…A handful of recent studies have employed such approaches in external fertilizers and reported complex patterns of multivariate selection on sperm phenotypes (Fitzpatrick, Simmons, & Evans, 2012; Johnson, Monro, & Marshall, 2013; Lymbery, Kennington, & Evans, 2018). For example, using an experimental approach that manipulated the size of gametes at fertilization, Monro and Marshall (2016) reported that egg and ejaculate size independently mediate patterns of selection on sperm morphology. However, we are unaware of any studies that have formally determined whether the form and direction of selection depend on external changes to sperm phenotypes, such as those induced by female‐derived chemicals, in a multivariate framework.…”

The thermal environment at fertilization mediates adaptive potential in the sea

“…Like many aquatic ectotherms, Galeolaria has sessile adults but planktonic gametes, embryos, and larvae, whose vulnerability to environmental stress makes them bottlenecks for population persistence under climate change (Pandori and Sorte 2019). Adult Galeolaria breed year‐round by spawning eggs and sperm into the external water column, where they must fuse for fertilization (Monro and Marshall 2016; Chirgwin et al. 2020), and where embryos and larvae also develop before eventually settling and recruiting into sessile adult populations.…”