Selection shapes turnover and magnitude of sex-biased expression in Drosophila gonads

Abstract

Background Sex-biased gene expression is thought to drive the phenotypic differences in males and females in metazoans. Drosophila has served as a primary model for studying male-female differences in gene expression, and its effects on protein sequence divergence. However, the forces shaping evolution of sex-biased expression remain largely unresolved, including the roles of selection and pleiotropy. Research on sex organs in Drosophila, employing original approaches and multiple-species contrasts, provides a means to gain insights into factors shaping the turnover and magnitude (fold-bias) of sex-biased expression. Results Here, using recent RNA-seq data, we studied sex-biased gonadal expression in 10,740 protein coding sequences in four species of Drosophila, D. melanogaster , D. simulans , D. yakuba and D. ananassae (5 to 44 My divergence). Using an approach wherein we identified genes with lineage-specific transitions (LSTs) in sex-biased status (amongst testis-biased, ovary-biased and unbiased; thus, six transition types) standardized to the number of genes with the ancestral state (S-LSTs), and those with clade-wide expression bias status, we reveal several key findings. First, the six categorical types of S-LSTs in sex-bias showed disparate rates of turnover, consistent with differential selection pressures. Second, the turnover in sex-biased status was largely unrelated to cross-tissue expression breadth, suggesting pleiotropy does not restrict evolution of sex-biased expression. Third, the fold-sex-biased expression, for both testis-biased and ovary-biased genes, evolved directionally over time toward higher values, a crucial finding that could be interpreted as a selective advantage of greater sex-bias, and sexual antagonism. Fourth, in terms of protein divergence, genes with LSTs to testis-biased expression exhibited weak signals of elevated rates of evolution (than ovary-biased) in as little as 5 My, which strengthened over time. Moreover, genes with clade-wide testis-specific expression (44 My), a status not observed for any ovary-biased genes, exhibited striking acceleration of protein divergence, which was linked to low pleiotropy. Conclusions By studying LSTs and clade-wide sex-biased gonadal expression in a multi-species clade of Drosophila, we describe evidence that interspecies turnover and magnitude of sex-biased expression have been influenced by selection. Further, whilst pleiotropy was not connected to turnover in sex-biased gonadal expression, it likely explains protein sequence divergence. Electronic supplementary material The online version of this article (10.1186/s12862-019-1377-4) contains supplementary material, which is available to authorized users.

Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

“…This pattern was also recently observed in red flour beetles (T. castaneum) [13]. The rapid divergence of male-biased genes has been proposed to be due to adaptive changes in amino acids arising from sexual selection pressures including male-male and sperm competition [4,[14][15][16], but could also reflect low pleiotropy that may relax purifying selection [7,10,[17][18][19]. Nonetheless, despite a persistent pattern of accelerated evolution of male-biased genes, an opposite pattern of rapid evolution of female-biased, including ovarybiased, genes has been found in some holometabolous insects, namely mosquitoes (Aedes, Anopheles) [20,21].…”

“…Sex-biased gene expression, and particularly male-biased gene expression, has been widely linked to rapid protein sequence evolution in studied animals (reviewed by (Ingleby et al, 2014, Grath & Parsch, 2016, Ellegren & Parsch, 2007)). In the insects, studies have largely focused on the holometabolous insect Drosophila , and have repeatedly shown the rapid evolution (high nonsynonymous to synonymous substitution rates, dN/dS) of male-biased genes, particularly those from the male sex cells or gonads, as compared to their female counterparts and/or to sexually unbiased genes (Haerty et al, 2007, Ellegren & Parsch, 2007, Jagadeeshan & Singh, 2005, Jiang & Machado, 2009, Zhang et al, 2007, Meisel, 2011, Grath & Parsch, 2012, Whittle & Extavour, 2019b, Perry et al, 2015) (but see also (Dorus et al, 2006)). This pattern was also recently observed for the gonads of red flour beetles ( T. castaneum ) (Whittle et al, 2020).…”

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

“…A further understanding of dosage compensation in this taxon may be achieved by attainment of transcriptional data from a wide range of individual somatic tissue types in T. castaneum , similar to analyses recently conducted in Drosophila [25]. Such multi-tissue expression data will also allow further assessments of cross-tissue pleiotropy of sex-biased genes [40, 57, 70] and may help further disentangle its role in constraining evolution of ovary-biased genes (Fig. 2).…”

Selection in males purges the mutation load on female fitness

“…The bulk of evidence in Drosophila and other organisms shows male-biased genes exhibiting high rates of nonsynonymous sequence and expression divergence among species (Meiklejohn et al 2003, Zhang Z. et al 2004, Zhang Z. and Parsch 2005, Metta et al 2006, Pröschel et al 2006, Zhang Y. et al 2007, Grath et al 2009, Assis et al 2012, Müller et al 2012, Harrison et al 2015, Dutoit et al 2018, Whittle and Extavour 2019. At first, this may not obviously accord with our findings/explanation (above) since these patterns can either be interpreted as stronger directional selection in males relative to females and/or relaxed purifying selection relative to femaleand un-biased genes (Ellegren and Parsch 2007, Meisel 2011, Parsch and Ellegren 2013 Wade 2016, Grath and Parsch 2016) -the latter seemingly incongruent.…”