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G3 (Bethesda). 2020 Jan 27. pii: g3.401074.2020. doi: 10.1534/g3.120.401074. [Epub ahead of print]

Absence of a Faster-X Effect in Beetles (Tribolium, Coleoptera).

Author information

1
Harvard University.
2
Harvard University extavour@oeb.harvard.edu.

Abstract

The faster-X effect, namely the rapid evolution of protein-coding genes on the X-chromosome, has been widely reported in metazoans. However, the prevalence of this phenomenon across diverse systems and its potential causes remain largely unresolved. Analysis of sex-biased genes may elucidate its possible mechanisms: for example, in systems with X/Y males a more pronounced faster-X effect in male-biased genes than in female-biased or unbiased genes may suggest 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. 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 a rarely observed absence of a faster-X effect in this organism. Further, analyses of sex-biased gene expression revealed that the X-chromosome was particularly highly enriched for ovary-biased genes, which evolved slowly. In addition, an evaluation of male X-chromosome dosage compensation in the gonads and in non-gonadal somatic tissues indicated a striking lack of compensation in the testis. This under-expression in testis may limit fixation of recessive beneficial X-linked mutations in genes transcribed in these male sex organs. Taken together, these beetles provide an example of the absence of a faster-X effect on protein evolution in a metazoan, that may result from two plausible factors, strong constraint on abundant X-linked ovary-biased genes and a lack of gonadal dosage compensation.

KEYWORDS:

Tribolium castaneum; dN/dS; dosage compensation; faster-X; sex-biased expression

PMID:
31988160
DOI:
10.1534/g3.120.401074
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