Multivariate Sexual Selection on Ejaculate Traits under Sperm Competition

Abstract

The widespread prevalence of sperm competition means that ejaculates face intense sexual selection. However, prior investigations of sexual selection on gametes have been hampered by two difficulties: (1) deriving estimates of relative fitness from sperm competition trials that are comparable across rival male and female genotypes and (2) obtaining measures of competitive fertilization success that are not confounded by postzygotic effects. Here, we exploit the experimental tractability of a broadcast spawning marine invertebrate to overcome these challenges and characterize multivariate sexual selection on sperm traits when multiple ejaculates compete. In multimale spawning events, we tracked real-time success of sperm using fluorescent tags that are visible inside fertilized eggs. We then used multivariate selection analyses to identify patterns of linear and nonlinear sexual selection on multiple sperm morphology and motility traits. Specifically, we found nonlinear selection against divergent combinations of sperm length, velocity, and swimming path linearity. These patterns likely reflect the way different swimming strategies allow sperm to locate and track eggs. Our results demonstrate that there are overall patterns of selection on ejaculates across a biologically realistic range of ejaculate-ejaculate and ejaculate-female interactions; therefore, there is the potential for adaptive evolution of ejaculate traits under sperm competition.

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, ).…”

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

“…Within a block, each individual male's fertilization success was assayed using pooled eggs from the same 4–6 females, thus minimizing the potential for male‐by‐female interaction effects in our measure of fertilization success (note that a different pool of females was used in each block). Previous work has confirmed that blocks of this size provide comparable estimates of fertilization ability among individual males across different pooled egg samples (Lymbery et al, 2018). Our total sample consisted of 23 blocks, comprising n = 138 males.…”

“…These observations of trait covariation suggest that ejaculate traits may be subject to both direct and indirect selection and correlational selection that favours particular combinations of traits, necessitating the use of multivariate analyses to separate components of selection (Blows, 2007; Lande & Arnold, 1983; Phillips & Arnold, 1989). 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.…”

“…For example, in M. galloprovincialis egg‐derived chemicals have been shown to alter several sperm traits, including swimming path direction, curvature and speed (Oliver & Evans, 2014) and cell physiology (Kekäläinen & Evans, 2017), all of which likely account for the findings that egg‐derived chemicals influence fertilization dynamics in this system (Evans, Garcia‐Gonzalez, Almbro, Robinson, & Fitzpatrick, 2012; Lymbery, Kennington, & Evans, 2017). Previous studies have reported overall variation in relative fitness among males and selection on complex combinations of sperm motility and morphological traits (Fitzpatrick et al, 2012; Lymbery et al, 2018). However, it is not known whether changes to sperm phenotypes elicited by the (female) fertilization environment influence these patterns of selection.…”