Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow

Abstract

Hybridization is increasingly recognized as an important evolutionary force contributing novel variation for selection to act on. While mis-expression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa and contributes novel variation remains an open question, especially for hybrid species without an increase in ploidy. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an old homoploid hybrid, Italian sparrow, Passer italiae. Through comparing the gene expression of parental species and F1 hybrids to that of the Italian sparrow, we find evidence for strongly transgressive expression in the Italian sparrow, with 22% of the testis genes exhibiting expression patterns outside the range of both parent species, compared to only 0.37% in the F1s. In contrast, Italian sparrow ovary expression was similar to that of one parent species, the house sparrow (P. domesticus). Moreover, the Italian sparrow testis transcriptome is 26.2 -26.6 times as diverged from those of the parent species compared to how divergent their transcriptomes are in spite of it being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in energy production and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions have molded the hybrid transcriptome.