Abstract
Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associated with a recently arisen, male-beneficial, X-linked mutation across tissues of the field cricket Teleogryllus oceanicus, and testing the relationship between the completeness of dosage compensation and female phenotypic effects at the level of gene expression. Dosage compensation in T. oceanicus was variable across tissues but usually incomplete, such that relative expression of X-linked genes was typically greater in females. Supporting the assumption that dosage compensation scales phenotypic effects between the sexes, we found tissues with incomplete dosage compensation tended to show female-skewed effects of the X-linked allele. In gonads, where expression of X-linked genes was most strongly female-biased, ovaries-limited genes were much more likely to be X-linked than were testes-limited genes, supporting the view that incomplete dosage compensation favours feminization of the X. Our results support the expectation that sex chromosome dosage compensation scales phenotypic effects of X-linked genes between sexes, substantiating a key assumption underlying the theoretical role of dosage compensation in determining the dynamics of sexual antagonism on the X.
Highlights
The X chromosome is widely predicted to be a hotspot for genes with sexually antagonistic fitness effects in XX/XY and XX/XO systems [1,2,3]
Recent theory has shown that the presence and completeness of dosage compensation are likely to play an important role in mediating sexual antagonism on the X [7,14], but the assumptions underlying this hypothetical role have rarely been addressed in empirical work
Theoretical studies have proposed that the degree of sex chromosome dosage compensation will influence the prevalence and dynamics of sexual antagonism on the X chromosome, traditionally viewed as a hotspot for genomic conflict between sexes [4], by scaling effects of X-linked alleles between sexes [7,14]
Summary
The X chromosome is widely predicted to be a hotspot for genes with sexually antagonistic fitness effects in XX/XY and XX/XO systems [1,2,3]. The role of allelic dominance in mediating these effects has been well studied, indicating sexual antagonism on the X should usually favour the spread of female-beneficial variants (as females transmit twice as many copies to the generation), unless recessive, in which case male-beneficial variants can more readily invade [4,5,6,7] These predictions could explain why genes with male-biased expression often appear underrepresented on X chromosomes [8,9,10,11]. We predicted that tissues exhibiting greater female-skew in gene expression effects of carrying the flatwing allele would be those with less complete dosage compensation (prediction 2) Such a pattern would support the interpretation that substantial female consequences of the male-beneficial flatwing allele are a consequence of incomplete dosage compensation, and that this should be an important parameter in predicting the spread of sexually antagonistic variants. Following our results from prediction 1, which reported little or no evidence of dosage compensation in sexually dimorphic gonads, we tested this by asking whether ovaries-limited genes were overrepresented on the X (prediction 3)
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