Support for the Dominance Theory in Drosophila Transcriptomes

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. 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, Drosophila 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 analyses also suggest a contribution of weakly deleterious regulatory mutations to gene expression divergence in genes with sex-biased expression, but only in the sex toward which the expression is biased (e.g., genes with female-biased expression when analyzed in females). In the opposite sex, we found stronger selective constraints on gene expression divergence. Although genes with a high degree of male-biased expression show a clear signal of faster-X evolution of gene expression, we also detected slower-X evolution in other gene classes (e.g., female-biased genes). This slower-X effect is mediated by significant decreases in cis- and trans-regulatory divergence. The distinct behavior of X-linked genes with a high degree of male-biased expression is consistent with these genes experiencing a higher incidence of positively selected regulatory mutations than their autosomal counterparts.