Nuclear transport genes recurrently duplicate by means of RNA intermediates in Drosophila but not in other insects

Abstract

Background The nuclear transport machinery is involved in a well-known male meiotic drive system in Drosophila. Fast gene evolution and gene duplications have been major underlying mechanisms in the evolution of meiotic drive systems, and this might include some nuclear transport genes in Drosophila. So, using a comprehensive, detailed phylogenomic study, we examined 51 insect genomes for the duplication of the same nuclear transport genes. Results We find that most of the nuclear transport duplications in Drosophila are of a few classes of nuclear transport genes, RNA mediated and fast evolving. We also retrieve many pseudogenes for the Ran gene. Some of the duplicates are relatively young and likely contributing to the turnover expected for genes under strong but changing selective pressures. These duplications are potentially revealing what features of nuclear transport are under selection. Unlike in flies, we find only a few duplications when we study the Drosophila duplicated nuclear transport genes in dipteran species outside of Drosophila, and none in other insects. Conclusions These findings strengthen the hypothesis that nuclear transport gene duplicates in Drosophila evolve either as drivers or suppressors of meiotic drive systems or as other male-specific adaptations circumscribed to flies and involving a handful of nuclear transport functions.

Testis- and ovary-expressedpolotranscripts and gene duplications affect male fertility when expressed in the germline

“…In addition, manipulating RanGTP in vertebrate oocytes affects meiosis II spindle assembly (Dumont et al 2007), demonstrating a sex-specific meiotic effect. Genes encoding nuclear transport proteins, such as RanGAP, are frequently duplicated, adaptively evolving, and thought to be important loci of genetic conflict (Betrán and Long 2003;Presgraves and Stephan 2007;Presgraves 2007;Tang and Presgraves 2009;Tracy et al 2010;Phadnis et al 2012;Mirsalehi et al 2021). The mechanisms by which RanGTP and other nuclear transport molecules affect male meiosis could be similar to how male germline expression of Plks affect sex chromosome transmission.…”

The roles of gene duplications in the dynamics of evolutionary conflicts

“…There is evidence that duplicated gene functions have repeatedly evolved tightly regulated expression and specialized function in the male germline [ 18 , 63 , 64 , 72 , 73 ]. The parental genes have been shown to be enriched for particular housekeeping functions including nuclear-encoded energy-related mitochondria genes in flies [ 66 ], glycolysis genes in mammals [ 74 , 75 ], transcription factors [ 76 , 77 ], ribosomal function [ 77 , 78 ], nuclear transport [ 19 , 21 , 79 ], proteasome subunits [ 80 ] or centromeric histones [ 22 ]. This reveals a functional role of these duplications independently of the known broad and potentially spurious expression of the genome in testes during histone-to-protamine transition [ 81 ] and independently of meiotic sex chromosome inactivation (MSCI; see below).…”

“…It has been proposed that MSCI might be the reason for this pattern [ 75 , 110 ]. However, the fact that not all housekeeping genes on the X are duplicated but only some that acquire specialized function for the male germline strongly supports the role of intralocus sexual antagonism resolution as the basis for this pattern [ 21 , 61 , 66 , 79 ]. Duplication plays a role in the spread of the dosage compensation marks on the X chromosome as the Y chromosome degenerates ( figure 5 b (iv)) and has been described to be mediated by TEs [ 101 , 113 ].…”