Gene Regulatory Evolution During Speciation in a Songbird

Abstract

Over the last decade, tremendous progress has been made toward a comparative understanding of gene regulatory evolution. However, we know little about how gene regulation evolves in birds, and how divergent genomes interact in their hybrids. Because of the unique features of birds - female heterogamety, a highly conserved karyotype, and the slow evolution of reproductive incompatibilities - an understanding of regulatory evolution in birds is critical to a comprehensive understanding of regulatory evolution and its implications for speciation. Using a novel complement of analyses of replicated RNA-seq libraries, we demonstrate abundant divergence in brain gene expression between zebra finch (Taeniopygia guttata) subspecies. By comparing parental populations and their F1 hybrids, we also show that gene misexpression is relatively rare among brain-expressed transcripts in male birds. If this pattern is consistent across tissues and sexes, it may partially explain the slow buildup of postzygotic reproductive isolation observed in birds relative to other taxa. Although we expected that the action of genetic drift on the island-dwelling zebra finch subspecies would be manifested in a higher rate of trans regulatory divergence, we found that most divergence was in cis regulation, following a pattern commonly observed in other taxa. Thus, our study highlights both unique and shared features of avian regulatory evolution.

Keywords: Dobzhansky-Muller; genome; inviability; reproductive isolation; sterility.

Figure 1

MA plot (expression level vs. log fold change) of differential expression for two contrasts. (A) Australian vs. Timor zebra finches and (B) Parental subspecies vs. their hybrids. Points in red are significant at P < 0.05 (adjusted for multiple testing). Larger point size in panel B is simply to increase visibility.

Figure 2

Six misexpressed genes in hybrid zebra finches. Statistics are based on differential expression comparison of the two zebra finch subspecies (n = 6) vs. their hybrids (n = 3) (Figure 1B). Five of these genes are significant at adjusted P < 0.05 and the sixth (TFIP11) is significant at adjusted P < 0.1 A, Australian; H, Hybrid; T, Timor.

Figure 3

Categorization of regulatory divergence modes based on patterns of allele-specific expression in hybrids and subspecific divergence. Most loci showed conserved expression (yellow). However, among those that show significant evidence of evolution, changes in cis regulation were most common (light blue). Less frequently observed categories are depicted with larger symbols to increase visibility.