Sex chromosome evolution: historical insights and future perspectives

Abstract

Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.

Keywords: degeneration; dosage compensation; heteromorphic; homomorphic; timeline; turnover.

Figure 1.

Overview of the dynamic evolution of sex chromosomes, illustrated in a male heterogametic system. Top left corner: an autosome pair in a hermaphrodite gains a sex-determining factor that evolves to become a highly heteromorphic pair of sex chromosomes, via cessation of recombination, degeneration (a) and evolution of dosage compensation (b). This progression can however be perturbed by a turnover event, such as the formation of a neo-sex chromosome (c) or a gain of a new sex-determining factor (d). In (c), the moderately degenerated Y chromosome fuses with an existing autosome, forming a new sex chromosome pair with an old sex-determining factor. In (d), an autosomal pair gains a new sex-determining factor, creating a completely new sex chromosome pair. The old Y is lost. In both (c) and (d), the old X may eventually gain diploidy through non-disjunction and subsequently lose dosage compensation, becoming an ordinary autosome pair. Figure adapted from [7]. Note that although (c) and (d) are shown as leading to chromosome turnovers, this progression is not inevitable. SA, sexually antagonistic allele.