Environment Influences Potential for Performance Legacies Across a Generation in a Reef Building Coral

Parental provisioning and transgenerational epigenetic inheritance are two mechanisms by which information from the environment experienced by the adults can be transmitted to offspring. This is particularly critical information for sessile, reef building corals, as environmental-performance mismatch can be detrimental, and preconditioning may provide beneficial acclimatory capacity. Here using a transplant experiment, we examined the impact of sites with differing thermal variance on the reproductive capacity (fecundity, egg size, eggs per bundle, and sperm motility) of adult Acropora hyacinthus colonies in Mo’orea French Polynesia, as well as mechanisms whereby environmental information can be transmitted across a generation (maternal egg mRNAs and sperm DNA methylation). A. hyacinthus colonies from the lower thermal variance forereef site had consistently higher fecundity, larger egg size, more eggs per bundle, and greater sperm motility compared to those transplanted to the backreef. Significant differentially expressed genes were apparent between the sites, demonstrating that environment during gametogenesis influenced maternal mRNA provisioning. Genes with greater expression levels in the high thermal variance backreef location included, for example, those associated with immune response (e.g., TNF receptor-associated factor 3-like and E3 ubiquitin-protein ligase MIB2-like) and thermotolerance (e.g., caseinolytic peptidase B protein). Sperm samples were analyzed with methyl binding domain enrichment and bisulfite sequencing (MBD-BS) to test the hypothesis of epigenetic inheritance. This study of reproductive performance, in combination with maternally-provisioned gene expression and paternally-inherited methylation patterns, provides a picture of how offspring performance is shaped across a generation by prior environmental history.