Ocean acidification during prefertilization chemical communication affects sperm success

Abstract

Ocean acidification (OA) poses a major threat to marine organisms, particularly during reproduction when externally shed gametes are vulnerable to changes in seawater pH. Accordingly, several studies on OA have focused on how changes in seawater pH influence sperm behavior and/or rates of in vitro fertilization. By contrast, few studies have examined how pH influences prefertilization gamete interactions, which are crucial during natural spawning events in most externally fertilizing taxa. One mechanism of gamete interaction that forms an important component of fertilization in most taxa is communication between sperm and egg‐derived chemicals. These chemical signals, along with the physiological responses in sperm they elicit, are likely to be highly sensitive to changes in seawater chemistry. In this study, we experimentally tested this possibility using the blue mussel, Mytilus galloprovincialis, a species in which females have been shown to use egg‐derived chemicals to promote the success of sperm from genetically compatible males. We conducted trials in which sperm were allowed to swim in gradients of egg‐derived chemicals under different seawater CO2 (and therefore pH) treatments. We found that sperm had elevated fertilization rates after swimming in the presence of egg‐derived chemicals in low pH (pH 7.6) compared with ambient (pH 8.0) seawater. This observed effect could have important implications for the reproductive fitness of external fertilizers, where gamete compatibility plays a critical role in modulating reproduction in many species. For example, elevated sperm fertilization rates might disrupt the eggs' capacity to avoid fertilizations by genetically incompatible sperm. Our findings highlight the need to understand how OA affects the multiple stages of sperm‐egg interactions and to develop approaches that disentangle the implications of OA for female, male, and population fitness.

Post-ejaculation thermal stress causes changes to the RNA profile of sperm in an external fertilizer

“…Spawning was induced by placing mussels in a heated water bath (28°C), as is standard for M. galloprovincialis ( [36], e.g. [49,50]).…”

“…These factors, as well as the tractability of M. galloprovincialis for spawning and gamete manipulation experiments (e.g. [35,36]), make it an excellent model system for exploring the effects of ocean warming on sperm. A previous study found that sperm of M. galloprovincialis appeared to maintain normal swimming behaviour and fertilization competence under short-term exposure to high temperatures [37], although decreased fertilization rates have also been reported at elevated temperatures [35].…”

Molecular mechanisms of sperm motility are conserved in an early-branching metazoan

“…This could be an important bottleneck for population fitness, as sperm activation and motility are vital for fertilization across metazoan phyla. Importantly, the response of sperm to ocean acidification is nuanced, as both positive and negative shifts in sperm performance have been observed at the level of the individual male in molluscs and echinoderms ( 77 – 80 ). This phenotypic diversity highlights the need to better understand the fundamental mechanisms that regulate sperm performance in order to predict how the fitness of corals and other marine invertebrates will be affected by a changing marine environment.…”

Molecular mechanisms of sperm motility are conserved in a basal metazoan

“…This could be an important bottleneck for population fitness, as sperm activation and motility are vital for fertilization across metazoan phyla. Importantly, the response of sperm to ocean acidification is nuanced, as both positive and negative shifts in sperm performance have been observed at the level of the individual male in molluscs and echinoderms (70)(71)(72)(73). This phenotypic diversity highlights the need to better understand the fundamental mechanisms that regulate sperm performance in order to predict how the fitness of corals and other marine invertebrates will be affected by a changing marine environment.…”