When and why does sex chromosome dosage compensation evolve?

Abstract

In many species, sex is determined by sex chromosomes, and the sex-specific chromosome (Y or W) stops recombining until it degenerates and carries fewer genes than its recombining counterpart (X or Z). This creates an imbalance in the dosage of most sex-linked genes between males and females. Early work in model organisms demonstrated that X chromosomes in multiple groups independently evolved regulatory mechanisms maintaining balanced expression of X-linked genes. However, recent studies have shown that these dosage compensation mechanisms are far from universal. It remains unclear why dosage compensation mechanisms evolved in some groups of organisms and not others. Two factors have led to confusion in this area: first, different authors sometimes define dosage compensation in different ways; second, dosage compensation is sometimes viewed as an all-or-nothing phenomenon, even though it may vary across cell types, developmental stages, and different classes of genes. Here, I discuss current approaches to testing for sex chromosome dosage compensation and highlight patterns in the phylogenetic distribution of dosage compensation mechanisms and possible explanations for those patterns. I conclude by outlining how the presence of dosage compensation can be tested in nearly any nonmodel organism and provide some recommendations for future studies.

The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence

“…Future work should further investigate if the regulators of sex determination and dosage compensation in flies (e.g., tra and Pof ) have similar roles in cockroach. An important limitation of our analysis is that we did not compare the same tissues between males and females [10,11]. Our inference of dosage compensation may be confounded by, for example, differences in cell types between tissues [69].…”

“…We next tested if the haploid dosage of element F homologs affects their expression in cockroach males. The ideal data to test for the effects of a haploid X are expression measurements from males and females from the same tissue and developmental stage [10,11]. Unfortunately, there are no available sex-matched RNA-seq gene expression datasets from German cockroach.…”

“…Despite the superficial similarities, the sex chromosomes and genes that initiate the sex determination pathways are not homologous between mammals and Drosophila [3]. In addition, some, but not all, animal taxa have evolved mechanisms to compensate for the haploid dose of the X chromosome in males, or Z chromosome in ZW females [8][9][10][11].…”

The microevolutionary response to male‐limited X‐chromosome evolution in Drosophila melanogaster reflects macroevolutionary patterns

“…Because males only have one copy of the X and females have two, males are expected to have half the expression at X‐linked loci as females do, all else being equal. In many species, this asymmetry in expression seems to be disadvantageous, since various forms of dosage compensation have evolved (Chandler, 2017). For example, female mammals inactivate one X‐chromosome, after which both sexes hyperexpress the X to maintain equal expression with the autosomes (Graves, 2016).…”

The microevolutionary response to male-limited X-chromosome evolution inDrosophila melanogasterreflects macroevolutionary patterns

“…Because males only have one copy of the X while females have two, males are expected to have half the expression at X-linked loci as females do, all else being equal. In many species this asymmetry in expression seems to be disadvantageous, since various forms of dosage compensation have evolved (Chandler 2017). For example, female mammals inactivate one X chromosome, after which both sexes hyperexpress the X to maintain equal expression with the autosomes (Graves 2016).…”