“Multivariate sexual selection on ejaculate traits under sperm competition”

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Rowan A. Lymbery, W. Jason Kennington, and Jonathan P. Evans (July 2018)

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We show patterns of multivariate selection on ejaculates, revealing potential for evolution under sperm competition

Sperm competition leads to selection on combinations of multiple ejaculate traits

The blue mussel (Mytilus galloprovincialis) in Perth, Western Australia. These mussels spawn in large aggregations, meaning sperm from multiple males compete to fertilize eggs.
(Credit: Rowan Lymbery)

In many species, the occurrence of female multiple mating (for internal fertilizers) or multi-individual spawning (for external fertilizers) leads to competition for fertilizations among ejaculates from rival males (sperm competition). Theory predicts that this should lead to sexual selection on ejaculate traits (e.g. sperm number, size, and speed) that provide males with a competitive advantage. However, it has traditionally been difficult to assess such patterns, for two reasons. First, competitive interactions often vary among different rival ejaculates, as well as between different ejaculates and females. This means estimates of a male’s competitive fertilization success are often relative to the specific rival ejaculates and females he is paired with, rather than reflecting a male’s overall fitness compared to the larger population. Second, it is typically challenging to identify which male’s sperm has been successful at fertilization. Therefore, competitive fertilization success is often estimated by offspring paternity, which can be confounded by post-fertilization factors (e.g., offspring viability).

In the current study, the authors overcome these challenges using a novel experimental system: the broadcast-spawning mussel Mytilus galloprovincialis. The authors replicated large multi-male, multi-female spawning events, and measured the competitive fertilization success of ejaculates from individual males using fluorescent sperm dyes. By using eggs and ejaculates from many individuals in each reproductive event, the authors provided realistic estimates of male reproductive fitness compared to the population. By measuring multiple ejaculate traits of each male, the study characterized complex patterns of multivariate selection on combinations of sperm size, speed, and swimming path straightness. Importantly, this study provides evidence that there are overall patterns of sexual selection on multiple ejaculate traits, and therefore the potential for adaptive evolution 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 post-zygotic effects. Here, we exploit the experimental tractability of a broadcast spawning marine invertebrate to overcome these challenges and characterise multivariate sexual selection on sperm traits when multiple ejaculates compete. In multi-male 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 non-linear sexual selection on multiple sperm morphology and motility traits. Specifically, we found non-linear 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.