Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)

Abstract

Genomewide analyses of the transcriptome have confirmed that gene misexpression may underlie reproductive isolation mechanisms in interspecific hybrids. Here, using a 16,006 features cDNA microarray, we compared and contrasted gene expression divergence at two ontogenetic stages in incipient species of normal and dwarf whitefish (Coregonus clupeaformis) with that of first generation (normal x dwarf) and second-generation hybrid crosses (backcross: [normal x dwarf] x normal]. Our goal was to identify the main mode of action responsible for gene transcription and to discover key genes misexpressed in hybrids. Very few transcripts (five of 4,950 expressed) differed in mean expression level between parentals and hybrids at the embryonic stage, in contrast to 16-week-old juvenile fish for which 617 out of 5,359 transcripts differed significantly. We also found evidence for more misexpression in backcross hybrids whereby nonadditivity explained a larger fraction of hybrid inheritance patterns in backcross (54%) compared with F1-hybrids (9%). Gene expression in hybrids was more variable than in pure crosses and transgressive patterns of expression were ubiquitous in hybrids. In backcross embryos in particular, the expression of three key developmental genes involved in protein folding and mRNA translation was severely disrupted. Accordingly, gene misexpression in hybrids adds to other factors previously identified as contributing to the reproductive isolation of incipient species of lake whitefish.