How to make a sex chromosome

Abstract

Sex chromosomes can evolve once recombination is halted between a homologous pair of chromosomes. Owing to detailed studies using key model systems, we have a nuanced understanding and a rich review literature of what happens to sex chromosomes once recombination is arrested. However, three broad questions remain unanswered. First, why do sex chromosomes stop recombining in the first place? Second, how is recombination halted? Finally, why does the spread of recombination suppression, and therefore the rate of sex chromosome divergence, vary so substantially across clades? In this review, we consider each of these three questions in turn to address fundamental questions in the field, summarize our current understanding, and highlight important areas for future work.

Figure 1. Sex chromosome strata.

Many plants and animals show evidence of strata, spatial clusters of X-Y, or Z-W, orthologs with similar divergence estimates. These spatial clusters are consistent with inversion events instantaneously halting recombination for all the encompassed loci. As inversions are proposed to occur in a stepwise process, strata differ in the length of time over which recombination has been suppressed. Therefore, orthologs with the largest neutral sequence divergence reside in the oldest stratum (shown in black), whereas those with the greatest sequence similarity are located in the youngest stratum (shown in white). The chicken Z chromosome (a) is comprised of at least four strata, formed over 130 million years and the human X chromosome (b) is comprised of at least five strata, although some recent analyses support six or more strata. The Silene X and Y chromosomes (c) diverged more recently and there is evidence for two strata over 10 million years. However, it is possible that orthology-based approaches underestimate the number of strata (regions unassigned to strata shown in green). For example, in highly degenerated regions, often all of the Y or W loci have decayed and no orthologs remain. In these cases, alternative methods have been used to identify additional strata.

Figure 2. Cartoon illustration of sex chromosome dosage compensation.

The decay of Y and W chromosome gene content leads to differences in gene dose (the number of gene copies) between the sexes. In male heterogamety (a,b) males have one half of the dose of all X-linked genes lost from the Y chromosome. In some cases, this difference in gene dose has led to the evolution of complete sex chromosome dosage compensation (a), where a mechanism acts across the chromosome to balance out the differences in gene dose, and as a consequence, the average expression for X-linked genes is equal in males and females. In many other cases (b), only some genes on the X are compensated, and the average expression from the X chromosome is less in males than females. In female heterogamety (c,d) females have one half of the dose of all Z-linked genes lost from the W chromosome. In some cases, this difference in gene dose has led to the evolution of complete sex chromosome dosage compensation (c), but in many other cases (d), only some genes on the Z are compensated, and the average expression from the Z chromosome is less in females than males.