Support for the dominance theory in Drosophila transcriptomes

Abstract

Interactions among divergent elements of transcriptional networks from different species can lead to misexpression in hybrids through regulatory incompatibilities, some with the potential to generate sterility. Genes with male-biased expression tend to be overrepresented among genes misexpressed in hybrid males. While the possible contribution of faster-male evolution to this misexpression has been explored, the role of the hemizygous X chromosome (i.e., the dominance theory for transcriptomes) remains yet to be determined. Here we study genome-wide patterns of gene expression in females and males of Drosophila yakuba and D. santomea and their hybrids. We used attached-X stocks to specifically test the dominance theory, and we uncovered a significant contribution of recessive alleles on the X chromosome to hybrid misexpression. Our analysis of gene expression patterns suggests that there is a contribution of weakly deleterious regulatory mutations to gene expression divergence in the sex towards which the expression is biased. In the opposite sex (e.g., genes with female-biased expression analyzed in male transcriptomes), we detect stronger selective constraints on gene expression divergence. Although genes with high degree of male-biased expression show a clear signal of faster-X evolution for gene expression divergence, we also detected slower-X evolution of gene expression in other gene classes (e.g. female-biased genes) that is mediated by significant decreases of cis- and trans-regulatory divergence. The distinct behavior of X-linked genes with high degree of male-biased expression is consistent with these genes experiencing a higher incidence of positively selected regulatory mutations than their autosomal counterparts. We propose that both dominance theory and faster-X evolution of gene expression may be major contributors to hybrid misexpression and possibly the large X-effect in these species.