Major disruption of gene expression in hybrids between young sympatric anadromous and resident populations of brook charr (Salvelinus fontinalis Mitchill)

Abstract

Genome-wide analyses of the transcriptome have suggested that male-biased genes are the first targets of genomic incompatibilities (g.i.) in inter-specific hybrids. However, those studies have almost invariably focused on Drosophila species that diverged at least 0.9 Ma, and with sterile male hybrids. Here, we use microarrays to analyse patterns of gene expression in very closely related (divergence <12,000 years), sympatric, but ecologically divergent anadromous and resident populations of brook charr (Salvelinus fontinalis) and their F(1) hybrids. Our results show a dramatic breakdown of gene expression patterns in hybrids compared with their parental relatives. Several disrupted genes are related to energetic metabolism, immune response, osmoregulation and protection against oxidative stress, and none has sex-biased functions. Besides, pure individuals show no expression differences at most of the genes disrupted in hybrids, which may suggest the operation of some form of stabilizing selection. Taken together, these results both confirm the idea that perturbations of regulatory networks represent a significant source of g.i. and support the suggestion that developmental pathways can diverge through time without any manifest change in the phenotypic outcome. While the role of other evolutionary forces (e.g. genetic drift) cannot be ruled out, this study suggests that ecological selective processes may provide the initial driving force behind disruption of gene expression in inter-specific hybrids.