Egg chemoattractants moderate intraspecific sperm competition

Abstract

Interactions among eggs and sperm are often assumed to generate intraspecific variation in reproductive fitness, but the specific gamete‐level mechanisms underlying competitive fertilization success remain elusive in most species. Sperm chemotaxis–the attraction of sperm by egg‐derived chemicals—is a ubiquitous form of gamete signaling, occurring throughout the animal and plant kingdoms. The chemical cues released by eggs are known to act at the interspecific level (e.g., facilitating species recognition), but recent studies have suggested that they could have roles at the intraspecific level by moderating sperm competition. Here, we exploit the experimental tractability of a broadcast spawning marine invertebrate to test this putative mechanism of gamete‐level sexual selection. We use a fluorescently labeled mitochondrial dye in mussels to track the real‐time success of sperm as they compete to fertilize eggs, and provide the first direct evidence in any species that competitive fertilization success is moderated by differential sperm chemotaxis. Furthermore, our data are consistent with the idea that egg chemoattractants selectively attract ejaculates from genetically compatible males, based on relationships inferred from both nuclear and mitochondrial genetic markers. These findings for a species that exhibits the ancestral reproductive strategy of broadcast spawning have important implications for the numerous species that also rely on egg chemoattractants to attract sperm, including humans, and have potentially important implications for our understanding of the evolutionary cascade of sexual selection.

Ocean acidification during prefertilization chemical communication affects sperm success

“…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).…”

“…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, ). However, whether OA alters these prefertilization processes has not yet been tested.…”

Assessing the potential for post‐ejaculatory female choice in a polyandrous beach‐spawning fish

“…We set up a series of 2 × 2 factorial crosses (n = 11), each involving two randomly selected females and males that were crossed in all four combinations (Table S2). This enabled us to evaluate the importance of interacting male-by-female effects, which would be consistent with cryptic female choice favouring specific males, mediated by substances in the female's cues (Evans, Garcia-Gonzalez, Almbro, Robinson, & Fitzpatrick, 2012;Lymbery et al, 2017;Poli et al, 2019;Rosengrave et al, 2008). Males and females were housed in separate holding tanks, and no attention was paid to body size during retrieval from the holding tanks.…”

“…However, emerging evidence from several taxa confirms that even with limited or no control over mating partners, females are able to exert considerable influence over fertilization using post-ejaculatory mechanisms of gamete selection (reviewed in Kekäläinen & Evans, 2018). For example, mytilid mussels have egg-derived chemical signals that can differentially bias competitive fertilization success towards genetically compatible male gametes (Lymbery, Kennington, & Evans, 2017). Similarly, the ovarian fluid of female ocellated wrasse (Symphodus ocellatus) changes the outcome of sperm competition by favouring males with preferred phenotypes who produce fewer but higher-quality sperm in sperm competition (Alonzo, Stiver, & Marsh-Rollo, 2016).…”

Effects of CXCL12/CXCR4/CXCR7 axis on human sperm motility and chemotaxis

“…The sperm-attracting substances secreted by female genital tract are called chemoattractant. After binding with specific sperm surface receptors, chemoattractant activates downstream pathways, increase the intracellular cAMP concentration and Ca 2+ influx, and accelerate sperm motility (Blengini et al, 2011; Lymbery et al, 2017). CXCL12 is a unique chemoattractant and plays an important role in the growth, metastasis and invasion of tumour cells (Esencay et al, 2013; Wang et al, 2015).…”