Should Y stay or should Y go: the evolution of non-recombining sex chromosomes

Abstract

Gradual degradation seems inevitable for non-recombining sex chromosomes. This has been supported by the observation of degenerated non-recombining sex chromosomes in a variety of species. The human Y chromosome has also degenerated significantly during its evolution, and theories have been advanced that the Y chromosome could disappear within the next ~5 million years, if the degeneration rate it has experienced continues. However, recent studies suggest that this is unlikely. Conservative evolutionary forces such as strong purifying selection and intrachromosomal repair through gene conversion balance the degeneration tendency of the Y chromosome and maintain its integrity after an initial period of faster degeneration. We discuss the evidence both for and against the extinction of the Y chromosome. We also discuss potential insights gained on the evolution of sex-determining chromosomes by studying simpler sex-determining chromosomal regions of unicellular and multicellular microorganisms.

Figure 1. Evolutionary trajectory of the non-recombining sex chromosome (using the human Y chromosome as an example)

The neo-X and Y chromosomes appeared about 160 million years ago (MYA), with each possessing about 1600 genes. While the X chromosome has not experienced significant degeneration, the Y chromosome has degraded significantly over time. This degradation is mainly due to the reduced population size that renders the Y chromosome prone to genetic drift, as well as reduces the efficiency of natural selection. The lack of natural selection was further enforced by the fact that meiotic recombination is suppressed across the majority of the Y chromosome (the black down arrows). On the other hand, there are factors that have been acting to counteract the degenerative forces and maintain the gene content of the Y chromosome. These include strong purifying selection, as well as gene conversions among copies of the duplicated genes that can homogenize the copies and maintain their sequence integrity (the green up arrows). The future of the human Y chromosome is still debated. The Y could still be on its way to complete degeneration (the black dashed line). Or it may be that the destructive and positive forces have reached equilibrium and the Y chromosome has achieved a stable status (the green dashed line). The red dashed line illustrates one of the possible evolutionary trajectories that the Y chromosome could have taken – a simple linear degradation. The degeneration of the Y chromosome could also be exponential, and occurred faster at the beginning and then slowed gradually. Another possible mode of degeneration is through a multi-stage process, taking into account a later addition of genes onto the human Y chromosome that occurred ~100 MYA (see [18,53]).