Ocean acidification does not overlook sex: Review of understudied effects and implications of low pH on marine invertebrate sexual reproduction

Abstract

Sexual reproduction is a fundamental process essential for species persistence, evolution, and diversity. However, unprecedented oceanographic shifts due to climate change can impact physiological processes, with important implications for sexual reproduction. Identifying bottlenecks and vulnerable stages in reproductive cycles will enable better prediction of the organism, population, community, and global-level consequences of ocean change. This article reviews how ocean acidification impacts sexual reproductive processes in marine invertebrates and highlights current research gaps. We focus on five economically and ecologically important taxonomic groups: cnidarians, crustaceans, echinoderms, molluscs and ascidians. We discuss the spatial and temporal variability of experimental designs, identify trends of performance in acidified conditions in the context of early reproductive traits (gametogenesis, fertilization, and reproductive resource allocation), and provide a quantitative meta-analysis of the published literature to assess the effects of low pH on fertilization rates across taxa. A total of 129 published studies investigated the effects of ocean acidification on 122 species in selected taxa. The impact of ocean acidification is dependent on taxa, the specific reproductive process examined, and study location. Our meta-analysis reveals that fertilization rate decreases as pH decreases, but effects are taxa-specific. Echinoderm fertilization appears more sensitive than molluscs to pH changes, and while data are limited, fertilization in cnidarians may be the most sensitive. Studies with echinoderms and bivalve molluscs are prevalent, while crustaceans and cephalopods are among the least studied species even though they constitute some of the largest fisheries worldwide. This lack of information has important implications for commercial aquaculture, wild fisheries, and conservation and restoration of wild populations. We recommend that studies expose organisms to different ocean acidification levels during the entire gametogenic cycle, and not only during the final stages before gametes or larvae are released. We argue for increased focus on fundamental reproductive processes and associated molecular mechanisms that may be vulnerable to shifts in ocean chemistry. Our recommendations for future research will allow for a better understanding of how reproduction in invertebrates will be affected in the context of a rapidly changing environment.

DNA methylation correlates with transcriptional noise in response to elevated pCO2in the eastern oyster (Crassostrea virginica)

“…These findings align with the growing consensus that gene body methylation may not have a direct regulatory role in gene-level expression, but instead functions to broadly reduce transcriptional variation across the genome [32,50,51]. Additionally, differences in gene activity and methylation patterns between female and male oysters highlight the need to examine how OA may affect reproduction differently in females and males [21], and underscore the cell- and tissue-specificity of DNA methylation [52,53].…”

“…Additional differences in female and male reproductive tissue responses to elevated pCO 2 underscore the importance of disentangling biological and environmental effects on gene expression and DNA methylation. It is well-known that OA can have sex-specific impacts on physiology [21], and previous work in C. gigas has documented distinct gene expression patterns associated with oogenesis and spermatogenesis [49]. We extend this work by demonstrating contrasting OA effects between female and male gonad tissues.…”

“…The ability of organisms to respond to and cope with OA are dependent on complex changes in whole-organism physiology, behavior, and molecular mechanisms [4,[18][19][20][21]. Additionally, plasticity, or the capacity for an organism to adjust their physiology to maintain function and performance in response to environmental change [22], is another important factor governing responses to OA.…”

Sex-biased gene expression precedes sexual dimorphism in the agonadal annelidPlatynereis dumerilii

“…Gametogenesis, the process of oocyte and sperm formation, is one of the fundamental processes of sexual reproduction, conferring genetic variability over generations and allowing species to propagate (Kikuchi and Tanaka, 2022; Nieuwkoop and Sutasurya, 1979; Padilla-Gamiño et al, 2022). This process involves a series of molecular events that orchestrate the differentiation of germ cells into mature gametes, either sperm or oocytes (Kikuchi and Tanaka, 2022).…”

Polystyrene Nanoplastics in Aquatic Microenvironments Affect Sperm Metabolism and Fertilization of Mytilus galloprovincialis (Lamark, 1819)

“…Species with external spawning, such as sessile marine invertebrates (bivalves), release their gametes into a marine microenvironment that is now perturbed by various stressors due to climate change (reduced PH, increased temperature) [1][2][3] and growing concentrations of various emerging contaminants (drugs, plastics, additives), concentrated over decades due to human negligence [4][5][6]. Currently, the scenario emerging from the literature is alarming due to the uncontrolled spread of plastics [7][8][9].…”