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Abstract
Males and females of the same species share the majority of their genomes, yet they are frequently exposed to conflicting selection pressures. Gene regulation is widely assumed to resolve these conflicting sex-specific selection pressures, and although there has been considerable focus on elucidating the role of gene expression level in sex-specific adaptation, other regulatory mechanisms have been overlooked. Alternative splicing enables different transcripts to be generated from the same gene, meaning that exons which have sex-specific beneficial effects can in theory be retained in the gene product, whereas exons with detrimental effects can be skipped. However, at present, little is known about how sex-specific selection acts on broad patterns of alternative splicing. Here, we investigate alternative splicing across males and females of multiple bird species. We identify hundreds of genes that have sex-specific patterns of splicing and establish that sex differences in splicing are correlated with phenotypic sex differences. Additionally, we find that alternatively spliced genes have evolved rapidly as a result of sex-specific selection and suggest that sex differences in splicing offer another route to sex-specific adaptation when gene expression level changes are limited by functional constraints. Overall, our results shed light on how a diverse transcriptional framework can give rise to the evolution of phenotypic sexual dimorphism.
Highlights
Males and females of many species can have divergent evolutionary optima, and are often subject to conflicting selection pressures (Andersson 1994), yet they share an almost identical set of genes
Splicing was estimated as the relative proportion of two alternative isoforms at each splice site, otherwise referred to as percent spliced-in (PSI)
S2, Supplementary Material online); skipped exons (SE), where an exon is either excluded or included from the mRNA, mutually exclusive exons (MXE), where one exon is skipped and the other is retained or vice versa, alternative 50 and 30 splice site events (A50SS and A30SS), where the exon boundary on either the 50- or 30-end of the intron is extended or shortened, and retained intron events, where a whole intron is retained in the final transcript
Summary
Males and females of many species can have divergent evolutionary optima, and are often subject to conflicting selection pressures (Andersson 1994), yet they share an almost identical set of genes. Genes with differences in expression level between males and females are pervasive across many species, and exhibit unique evolutionary properties, including faster rates of sequence and expression evolution (Ranz et al 2003; Khaitovich et al 2005; Ellegren and Parsch 2007; Harrison et al 2015). These genes have been the subject of considerable focus in understanding how selection can navigate the constraints imposed by a shared genome, and the consequences for sex-specific adaptation (Mank 2017a, 2017b).
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