Paternal diet shapes paternal and maternal transcriptomes in the early embryo through parallel sperm-associated mechanisms

Life experiences in fathers can influence phenotypes in the offspring. While it is known that acquired paternal information can be transferred to descendants via the germline, how such transfer operates between sperm and embryo remains unclear. We examined the effects of low protein diet (LPD) on males of different genotypes and their hybrid offspring generated by reciprocal outcross and on their genome. We found that LPD induces genotype-specific effects in fathers and different phenotypes in their male and female offspring. Allele-specific analyses revealed that paternal LPD modifies paternal and maternal transcriptomes differently in early two-cell embryos. Changes in the paternal transcriptome overlap with the sperm transcriptome and are associated with sperm chromatin features, suggesting that sperm-inherited transcripts and chromatin states may shape the paternal transcriptome in the embryo. The maternal transcriptome, by contrast, is linked to sperm-derived small RNAs, consistent with a possible role of sperm-derived small RNAs in modulating maternal transcript levels in the embryo. Analyses of undifferentiated spermatogonia populations suggest that LPD-induced sperm states can originate from early stages of germ cells. These findings provide evidence that paternal experiences can influence the early embryo via processes involving each parental allele differently.