Convergently recruited nuclear transport retrogenes are male biased in expression and evolving under positive selection in Drosophila

Abstract

The analyses of gene duplications by retroposition have revealed an excess of male-biased duplicates generated from X chromosome to autosomes in flies and mammals. Investigating these genes is of primary importance in understanding sexual dimorphism and genome evolution. In a particular instance in Drosophila, X-linked nuclear transport genes (Ntf-2 and ran) have given rise to autosomal retroposed copies three independent times (along the lineages leading to Drosophila melanogaster, D. ananassae, and D. grimshawi). Here we explore in further detail the expression and the mode of evolution of these Drosophila Ntf-2- and ran-derived retrogenes. Five of the six retrogenes show male-biased expression. The ran-like gene of D. melanogaster and D. simulans has undergone recurrent positive selection. Similarly, in D. ananassae and D. atripex, the Ntf-2 and ran retrogenes show evidence of past positive selection. The data suggest that strong selection is acting on the origin and evolution of these retrogenes. Avoiding male meiotic X inactivation, increasing level of expression of X-linked genes in male testes, and/or sexual antagonism might explain the recurrent duplication of retrogenes from X to autosomes. Interestingly, the ran-like in D. yakuba has mostly pseudogenized alleles. Disablement of the ran-like gene in D. yakuba indicates turnover of these duplicates. We discuss the possibility that Dntf-2r and ran-like might be involved in genomic conflicts during spermatogenesis.

Figure 1.—

qRT–PCR results for the D. ananassae and D. grimshawi retrogenes (Da_ran-like, Da_Ntf-2r, Dg_ran-like, and Dg_ Ntf-2r) are shown. The average of the retrogene C_T difference to the normalizing gene (i.e., ΔC_T) and standard errors are shown for every tissue type. f, females; m, males.

Figure 2.—

Alignment of ran and Drosophila ran-like proteins highlighting amino acid residues of known function. Arrows point to sites that have likely been under positive selection in the retrocopies (Table 2).