Additive and non-additive epigenetic signatures of hybridisation between fish species with different mating systems

Abstract

Hybridisation is a major source of evolutionary innovation. However, several prezygotic and postzygotic factors influence its likelihood and evolutionary outcomes. Differences in mating systems can have a major effect on the extent and direction of hybridisation and introgression. In plants, epigenetic mechanisms help to stabilize hybrid genomes and contribute to reproductive isolation, but the relationship between genetic and epigenetic changes in animal hybrids is unclear. We analysed the extent of a unique case of natural hybridisation between two genetically distant mangrove killifish species with different mating systems, Kryptolebias hermaphroditus (self-fertilising) and K. ocellatus (outcrossing), and the methylation patterns of their hybrids. Hybridisation rate between the species ranged between 14% and 26%. Although co-existing parental species displayed highly distinct genetic (microsatellites and SNPs) and methylation patterns (37,000 differentially methylated cytosines), our results indicate that F1 hybrids are viable and able to backcross with parental species. Hybrids had predominantly intermediate methylation patterns (88.5% of the sites) suggesting additive effects, as expected from hybridisation between genetically distant species. Differentially methylated cytosines between hybrids and both parental species (5,800) suggest that introgressive hybridisation may play a role in generating novel genetic and epigenetic variation which could lead to species diversification. We also found a small percentage of non-additive epigenetic effects which might act as an evolutionary bet-hedging strategy and increase fitness under environmental change.