Tissue-specific patterns of regulatory changes underlying gene expression differences among Ficedula flycatchers and their naturally occurring F 1 hybrids

Changes in interacting - and -regulatory elements are important candidates for Dobzhansky-Muller hybrid incompatibilities and may contribute to hybrid dysfunction by giving rise to misexpression in hybrids. To gain insight into the molecular mechanisms and determinants of gene expression evolution in natural populations, we analyzed the transcriptome from multiple tissues of two recently diverged flycatcher species and their naturally occurring F hybrids. Differential gene expression analysis revealed that the extent of differentiation between species and the set of differentially expressed genes varied across tissues. Common to all tissues, a higher proportion of Z-linked genes than autosomal genes showed differential expression, providing evidence for a fast-Z effect. We further found clear signatures of hybrid misexpression in brain, heart, kidney, and liver. However, while testis showed the highest divergence of gene expression among tissues, it showed no clear signature of misexpression in F hybrids, even though these hybrids were found to be sterile. It is therefore unlikely that incompatibilities between - regulatory changes explain the observed sterility. Instead, we found evidence that -regulatory changes play a significant role in the evolution of gene expression in testis, which illustrates the tissue-specific nature of -regulatory evolution bypassing constraints associated with pleiotropic effects of genes.