Does post-ejaculatory sperm experience prior to fertilization alter offspring performance beyond paternity in an external fertilizing fish?

Abstract

Recent research has suggested that the environment encountered by sperm post-ejaculation may impact offspring development beyond the transfer of the paternal genome. The mechanisms that underlie such effects remain unclear, but two non-mutually exclusive processes have been proposed. 1) Haploid selection, whereby stressful conditions act as stronger post-ejaculation pre-fertilization selective pressures on semen than under benign situations, resulting in the fertilization of, on average higher quality sperm and the production of offspring that exhibit superior performance across all environmental conditions that they might encounter. 2) Epigenetic inheritance, where environmental conditions induce changes in sperm that are passed down to offspring, resulting in altered gene expression in offspring. This would be adaptive if sperm experiences anticipate what is to come and improve offspring performance to match those conditions. Capelin (Mallotus villosus) sperm and embryos are sensitive to salinity and may represent a good system to investigate these phenomena. We used a split-ejaculate and split-brood experimental block design to expose capelin sperm to known benign (25 psu) and stressful (35 psu) salinity prior to egg contact, and split each batch of fertilized eggs for incubation at matched and mismatched salinity to those of sperm exposure. Our findings revealed no differences in hatch characteristics between offspring produced by sperm exposed to benign and stressful salinity conditions. A follow-up experiment found the same result with an increased selection gradient at 5 psu and 35 psu. Our study does not support the hypothesis that sperm experiences exert an influence on the development of offspring characteristics, independent of paternity. Instead, our results suggest that the sole influential factor in sperm determining offspring characteristics is the transfer of the paternal genome.