Absence of a faster-X effect in beetles (Tribolium, Coleoptera)

Background The faster-X effect, namely the rapid evolution of protein-coding genes on the X-chromosome, has been reported in numerous metazoans. However, the prevalence of this phenomenon across metazoans and its potential causes remain largely unresolved. Analysis of sex-biased genes may elucidate its possible mechanisms: a more pronounced faster-X effect in male-biased genes than in female-biased or unbiased genes, suggests fixation of recessive beneficial mutations rather than genetic drift. Further, theory predicts that the faster-X effect should be promoted by X-chromosome dosage compensation, but this topic remains rarely empirically examined. Results Here, we asked whether we could detect a faster-X effect in genes of the beetle Tribolium castaneum (and T. freemani orthologs), which has X/Y sex-determination and heterogametic males. Our comparison of protein sequence divergence (dN/dS) on the X-chromosome versus autosomes indicated the complete absence of a faster-X effect. Further, analyses of sex-biased gene expression revealed that the X-chromosome was strongly enriched for ovary-biased genes, which evolved under exceptionally high constraint. An evaluation of male X-chromosome dosage compensation in the gonads and in non-gonadal somatic tissues showed an extreme lack of compensation in the testis. This under-expression of the X chromosome in males may limit the phenotypic effect, and therefore likelihood of fixation, of recessive beneficial X-linked mutations in genes transcribed in male gonads. Conclusions We show that these beetles display a rare unequivocal example of the absence of a faster-X effect in a metazoan. We propose two potential causes for this, namely high constraint on X-linked ovary-biased genes, and an extreme lack of dosage compensation of genes transcribed in the testis.