The evolution of sex-biased gene expression in theDrosophilabrain

Abstract

Genes with sex-biased expression in Drosophila are thought to underlie sexually dimorphic phenotypes and have been shown to possess important evolutionary properties. However, the forces and constraints governing the evolution of sex-biased genes in the somatic tissues of Drosophila are largely unknown. Using population-scale RNA sequencing data we show that sex-biased genes in the Drosophila brain are highly enriched on the X Chromosome and that most are biased in a species-specific manner. We show that X-linked male-biased genes, and to a lesser extent female-biased genes, are enriched for signatures of directional selection at the gene expression level. By examining the evolutionary properties of gene flanking regions on the X Chromosome, we find evidence that adaptive cis-regulatory changes are more likely to drive the expression evolution of X-linked male-biased genes than other X-linked genes. Finally, we examine whether constraint due to broad expression across multiple tissues and genetic constraint due to the largely shared male and female genomes could be responsible for the observed patterns of gene expression evolution. We find that expression breadth does not constrain the directional evolution of gene expression in the brain. Additionally, we find that the shared genome between males and females imposes a substantial constraint on the expression evolution of sex-biased genes. Overall, these results significantly advance our understanding of the patterns and forces shaping the evolution of sexual dimorphism in the Drosophila brain.

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

“…3A, Table 1). While the study of protein evolution of sex-biased brain genes (brains sensu stricto , rather than simply heads, or pooled brain-eye tissues as considered by some previous studies (Catalan et al, 2018, Congrains et al, 2018)) remains rare, rapid evolution of female-biased brain genes has been reported in some bird embryos (Mank et al, 2007), and in some autosomal genes in flies (Khodursky et al, 2020). However, an opposite pattern of rapid evolution of male-biased brain genes for several stages of development was reported in humans (Shi et al, 2016).…”

“…The brain is a major tissue type providing the neurological basis for the mating behaviors of courtship, intrasex competition, mate-choice, and post-mating male-female responses (Wright & Mank, 2013, Mank et al, 2007, Dalton et al, 2010, Naurin et al, 2011). Male and female differences in gene expression per se in the brain have been examined in some insects and vertebrates (Mank et al, 2007, Small et al, 2009, Santos et al, 2008, Naurin et al, 2011, Catalan et al, 2012, Shi et al, 2016, Tomchaney et al, 2014, Ingleby et al, 2014, Wright & Mank, 2013, Yang et al, 2016, Jagadeeshan & Singh, 2005, Khodursky et al, 2020, Huylmans & Parsch, 2015). Further, in Drosophila , analyses of a small number of neural genes are directly connected to mating functions and behaviors (Drapeau et al, 2003, Kadener et al, 2006, Dauwalder, 2008).…”

“…However, there is a striking paucity of data on whether and how sex-biased expression in the brain is associated with protein sequence evolution (Mank et al, 2007;Wright & Mank, 2013). Moreover, the minimal research available from birds, humans and flies has suggested that male and female expression may have different effects on the rates of protein evolution, depending on the system (Mank et al, 2007;Shi et al, 2016;Khodursky et al, 2020) (see also some brain-related (Biswas et al, 2016) and composite-tissue analyses (Catalan et al, 2018;Congrains et al, 2018)), and the causes of those patterns remain poorly understood. It is therefore evident that additional study of sex-biased expression in the brain is needed, particularly with respect to its relationship to molecular evolution.…”

High rates of evolution preceded shifts to sex-biased gene expression inLeucadendron, the most sexually dimorphic angiosperms

“…Reflecting the notion that directional selection should both increase divergence between groups and decrease variation in the group under selection, delta-x takes higher values the higher divergence and the lower polymorphism. Low expression polymorphism relative to interspecific divergence is a hallmark of adaptive evolution (Nuzhdin et al 2004;Ometto et al 2011;Khodursky et al 2020).…”