Female-induced remote regulation of sperm physiology may provide opportunities for gamete-level mate choice

Abstract

In sedentary externally fertilizing species, direct interactions between mating partners are limited and prefertilization communication between sexes occurs largely at the gamete level. Certain combinations of eggs and sperm often have higher fertilization success than others, which may be contingent on egg-derived chemical factors that preferentially attract sperm from compatible males. Here, we examine the mechanisms underlying such effects in the marine mussel Mytilus galloprovincialis, where differential sperm attraction has recently been shown to be associated with variation in offspring viability. Specifically, we focus on the sperm surface glycans, an individually unique layer of carbohydrates that moderate self-recognition and other cellular-level interactions. In many species egg-derived factors trigger remarkable changes in the sperm's glycan layer, physiology, and swimming behavior, and thus potentially moderate mate choice at the gamete level. Here, we show that sperm glycan modifications and the strength of acrosome reaction are both dependent on specific male-female interactions (male-female combination). We also find associations between female-induced sperm glycan changes and the Ca influx into sperm--a key regulator of fertilization processes from sperm capacitation to gamete fusion. Together, our results suggest that female-induced remote regulation of sperm physiology may constitute a novel mechanism of gamete-level mate choice.

Ocean acidification during prefertilization chemical communication affects sperm success

“…To date, only a few EC molecules have been identified in broadcast spawning species (e.g., Böhmer et al, ; Riffell, Krug, & Zimmer, ; Ward, Brokaw, Garbers, & Vacquier, ; Yoshida, Murata, Inaba, & Morisawa, ) and we currently have no information in this regard for M. galloprovincialis . Furthermore, it would be interesting to examine the effect of OA on EC‐induced changes in sperm physiology, for example, pH i changes and influx of calcium when mixed with ECs (e.g., see the techniques used in Kekäläinen & Evans, ; Kekäläinen, Larma, Linden, & Evans, ). Such studies would provide a detailed understanding of cellular and biochemical processes underlying the effects of OA on gamete interactions.…”

“…Instead, the fitness consequences of OA will depend on whether the observed effect disrupts the capacity of eggs to promote fertilizations by preferred sperm. In M. galloprovincialis, females use ECs to differentially regulate sperm movement and physiology (Evans et al, 2012;Kekäläinen & Evans, 2016;Oliver & Evans, 2014)-processes that ultimately favor sperm from genetically compatible males when multiple ejaculates compete for fertilization (as is likely in realistic mass spawning events) (Lymbery et al, 2017). This form of gamete-mediated mate choice provides benefits to females in terms of enhanced offspring viability (Oliver & Evans, 2014 Kekäläinen, Larma, Linden, & Evans, 2015).…”

“…For example, a series of recent studies on M. galloprovincialis has revealed complex effects of egg‐derived chemicals (ECs) in the seawater on subsequent sperm success. These studies demonstrated that, among intraspecific male–female pairings, ECs differentially moderate patterns of sperm attraction (Evans, García‐González, Almbro, Robinson, & Fitzpatrick, ), swimming behavior (Oliver & Evans, ), and changes to sperm surface physiology (e.g., acrosome reaction and arrangement of glycan molecules; Kekäläinen & Evans, ). These effects of ECs on sperm behavior and physiology are likely to explain how females regulate fertilization in favor of genetically compatible males when ejaculates from different males compete (Lymbery, Kennington, & Evans, ).…”

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

“…; Crean et al. ; Kekäläinen and Evans ). Likewise, cryptic female choice for sperm of compatible mates in an intermale competition scenario has been demonstrated, however, only at the individual level (Olsson et al.…”

Post‐ejaculatory modifications to sperm (PEMS)

“…Failure to modify sperm properly could be a general and widespread mechanism by which females discriminate against the sperm of less‐preferred males, as has been shown to be the case with sperm chemoattraction (Kekäläinen & Evans, ) and with female sperm ejection and sperm digestion (Manier et al ., ; Firman et al ., ). Similarly, two kinds of studies implicate a role for ovarian fluid in mediating sexual selection within populations.…”