The thermal environment of sperm affects offspring success: a test of the anticipatory paternal effects hypothesis in a broadcast spawner

There has been an explosion of recent evidence that environments experienced by fathers or their ejaculates can influence offspring phenotypes (paternal effects). However, little is known about whether such effects are adaptive, which would have far-reaching implications for the many species facing rapidly changing environments. For example, some arguments suggest paternal effects might be a source of cross-generational plasticity, preparing offspring to face similar conditions to their father (anticipatory hypothesis). Alternatively, ejaculate-mediated effects on offspring may be non-adaptive by-products of stress. Here, we conduct an experiment to distinguish between these predictions, exposing ejaculates of the externally fertilizing mussel Mytilus galloprovincialis to ambient (19 °C) and high (24 °C) temperatures, then rearing offspring groups in temperatures that match and mismatch those of sperm. We find that, overall, high-treated sperm induced higher rates of normal offspring development, and higher success in transitioning to second-stage larvae, which may represent adaptive epigenetic changes or selection on sperm haplotypes. However, progeny of high-treated sperm did not perform better than those of ambient-treated sperm when rearing temperatures were high. Overall, these findings offer little support for anticipatory hypothesis and suggest instead that beneficial paternal effects may be eroded when offspring develop under stressful conditions.

Methods
These data were collected from an experiment testing whether ejaculate-mediated paternal effects of temperature are adaptive for offspring, using the externally fertilizing mussel Mytilus galloprovincialis. Mussels were induced to spawn, and ejaculates from males (n = 34) were split into two aliquot; one aliquot was exposed to ambient temperature (19 °C) and the other to high temperature (24 °C). The aliquots were used to fertilise separate batches of pooled eggs (i.e., eggs pooled from mulriple females), and fertilization rates measured after 2 h. Each batch of eggs was then split into two aliquots that were exposed to different rearing temperatures over 48 h; again using ambient (19 °C) and high (24 °C) temperature treatments. After 48 h, the number of surviving offspring was counted, along with the proportion that were trocophore (first-stage) vs. veliger (second-stage) larvae and the portion that exhibited normal vs. abnormal morphology and swimming.