Gene expression in natural F1 hybrids of Ficedula flycatchers and their parental species

Recent evidence suggests that changes in interacting cis- and trans-regulatory elements may be important candidates for Dobzhansky-Muller hybrid incompatibilities, and can contribute to hybrid dysfunction by giving rise to mis-expression in hybrids. To gain insight into the molecular mechanisms and determinants of gene expression evolution in natural populations, we analysed the transcriptome from multiple tissues of two recently diverged Ficedula flycatcher species and their naturally-occurring F1 hybrids. Differential gene expression analysis revealed that the extent of differentiation between species and the set of differentially expressed genes differed across tissues. Nevertheless, common to all tissues, a higher proportion of Z-linked genes than autosomal genes showed differential expression. We further found clear signatures of hybrid mis-expression in brain, heart, kidney and liver, suggesting a role of Dobzhansky-Muller hybrid incompatibilities between divergent regulatory elements in these tissues. While testis showed the highest divergence of gene expression among tissues, it showed no clear signature of mis-expression in F1 hybrids. Instead, we found evidence that cis-regulatory changes play a significant role in the evolution of gene expression in testis, which illustrates the tissue-specific nature of cis-regulatory evolution bypassing the constraints associated with pleiotropic effects of genes.