The interaction between microbiome and epigenetic diversity as a source of phenotypic variation for fish with low genetic diversity

Abstract Non-genetic sources of phenotypic variation, such as the epigenome and the microbiome, could be important sources of adaptive variation for species with low genetic diversity, but little is known about the complex interaction between them and the genetic diversity of the host, particularly in wild populations. We examined the skin microbiome composition of two closely related mangrove killifish species with different mating systems (self-fertilising and outcrossing) under sympatric and allopatric conditions, to partition the influence of the genotype and the environment on their microbiome and epigenetic profiles. The diversity and community composition of the skin microbiome were shaped by strong genotype by environment interactions. We also found positive relationships between individual genetic diversity (heterozygosity) and microbiome alpha diversity (Faith and Chao1 measures) and between epigenetic variation and alpha diversity (Simpson evenness). Individual pairwise epigenetic and microbiome differentiation were positively correlated and influenced by species. We propose that the interaction between the host genotype, the microbiome and the epigenome can provide a plastic response to environmental variation, particularly relevant for individuals with low genetic diversity, and highlight the importance of considering the holobiont as the unit of selection to understand adaptation to environmental change.