Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate

Abstract

In numerous species, egg chemoattractants play a critical role in guiding sperm towards unfertilized eggs (sperm chemotaxis). Until now, the known functions of sperm chemotaxis include increasing the effective target size of eggs, thereby promoting sperm–egg encounters, and facilitating species recognition. Here, we report that in the broadcast spawning mussel, Mytilus galloprovincialis , egg chemoattractants may play an unforeseen role in sexual selection by enabling sperm to effectively ‘choose’ between the eggs of different conspecific females. In an initial experiment, we confirmed that sperm chemotaxis occurs in M. galloprovincialis by showing that sperm are attracted towards unfertilized eggs when given the choice of eggs or no eggs in a dichotomous chamber. We then conducted two cross-classified mating experiments, each comprising the same individual males and females crossed in identical male × female combinations, but under experimental conditions that offered sperm ‘no-choice’ (each fertilization trial took place in a Petri dish and involved a single male and female) or a ‘choice’ of a female's eggs (sperm were placed in the centre of a dichotomous choice chamber and allowed to choose eggs from different females). We show that male-by-female interactions characterized fertilization rates in both experiments, and that there was remarkable consistency between patterns of sperm migration in the egg-choice experiment and fertilization rates in the no-choice experiment. Thus, sperm appear to exploit chemical cues to preferentially swim towards eggs with which they are most compatible during direct sperm-to-egg encounters. These results reveal that sperm differentially select eggs on the basis of chemical cues, thus exposing the potential for egg chemoattractants to mediate mate choice for genetically compatible partners. Given the prevalence of sperm chemotaxis across diverse taxa, our findings may have broad implications for sexual selection in other mating systems.

Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate

“…egg choice) revealed significant male-by-female interaction effects (table 2). Thus, consistent with previous findings for this species [22], the strength of chemically moderated gamete preferences was contingent on the specific identities of eggs and sperm present in each trial. Similarly, in the no-choice assays, fertilization rates, larval survival and the two composite measures of sperm motility (PC1 and PC2) were influenced by the interacting effects of male and female identities (table 2).…”

“…This study adds two key findings to these previous analyses. First, we show that there are measurable fitness benefits associated with these chemically moderated gamete preferences; sperm preferentially swim towards eggs that not only deliver higher fertilization rewards (this study and [22]) but also those that yield higher post-zygotic survival rates. In other contexts, previous studies have reported significant male-by-female interactions at fertilization [33,34], but the question of whether 'compatible' combinations of sperm and eggs yield high post-zygotic survival has received less attention, and some studies investigating this topic in other contexts have reported no significant association between fertilization and offspring viability [23 -25].…”

“…178C to match ambient seawater temperatures) before use. Note that this marine population differs from the (estuarine) population tested previously to reveal differential sperm chemoattraction in this species [22]. Spawning was induced by temperature shock by transferring mussels from their holding tanks into 60 Â 37 Â 37 cm plastic containers filled with approximately 6 cm of seawater preheated to 308C [26].…”

“…Although traditionally explained as a mechanism for maximizing gamete encounter rates and ensuring conspecific fertilizations (reviewed in [21]), recent evidence suggests that sperm chemoattraction may also function to select compatible gametes. In the mussel Mytilus galloprovincialis, sperm that are simultaneously exposed to egg chemoattractants coming from two different females display consistent but differential 'preferences' for eggs that confer high fertilization rates in subsequent (nochoice) crosses [22]. Although this finding is consistent with the intriguing possibility that egg chemoattractants play a role in the selection of genetically compatible mates, the extent to which differential gamete preferences influence offspring survival has never been investigated.…”

Status Specific Tailoring of Sperm Behavior in an External Fertilizer

“…However, disentangling the separate effects of varying quality of sperm and differing ovarian fluids on fertilization success and offspring quality under sperm competition is challenging. Some authors have demonstrated positive effects of ovarian fluid on sperm velocity (Gasparini and Pilastro, 2011;Evans et al, 2012;Oliver and Evans, 2014;Alonzo et al, 2016;Rosengrave et al, 2016), while Lumley et al (2016) revealed no effect of ovarian fluid on relative offspring fitness. Moreover, the only published intraspecific study exchanging ovarian fluid between eggs from different females documented no overall effect of ovarian fluid on paternity success under sperm competition and no evidence for male-female interactions (Evans et al, 2013).…”