When and how do sex‐linked regions become sex chromosomes?

Abstract

The attention given to heteromorphism and genetic degeneration of "classical sex chromosomes" (Y chromosomes in XY systems, and the W in ZW systems that were studied first and are best described) has perhaps created the impression that the absence of recombination between sex chromosomes is inevitable. I here argue that continued recombination is often to be expected, that absence of recombination is surprising and demands further study, and that the involvement of selection in reduced recombination is not yet well understood. Despite a long history of investigations of sex chromosome pairs, there is a need for more quantitative approaches to studying sex-linked regions. I describe a scheme to help understand the relationships between different properties of sex-linked regions. Specifically, I focus on their sizes (differentiating between small regions and extensive fully sex-linked ones), the times when they evolved, and their differentiation, and review studies using DNA sequencing in nonmodel organisms that are providing information about the processes causing these properties.

Y recombination arrest and degeneration in the absence of sexual dimorphism

“…There is ample evidence for sexual conflict in general, making this assumption plausible. However, the role of SA-loci in Y recombination arrest is not demonstrated empirically (3,5,26,27). This demonstration is inherently difficult to make because SA-loci are difficult to detect and because they can occur after the recombination arrest.…”

“…Current theory proposes that Y chromosomes evolve through three steps. Step 1 is a consequence of the evolution of sexual dimorphism ( 9 ): divergent selection in males and females may generate intralocus sexual conflict, which, for loci linked to a sex-determining locus, favours suppressed recombination, so that the allele favorable in one sex becomes associated with that sex ( 6 – 13 ). In the second step, selective interference in the absence of recombination reduces the efficacy of natural selection, leading to accumulation of deleterious mutations on the Y and genetic degeneration.…”

“…years, both empirically and theoretically (5,6,(21)(22)(23)(24)(25). Empirical support for the first step is particularly equivocal where despite decades of investigation (3,5,26,27), decisive evidence for a causal role of sexually-antagonistic loci on recombination arrest, is conspicuously lacking. The second step is difficult to reconcile with the observation of small degenerated strata (5), within which selective interference should be minimal.…”

“…Empirical support for the first step is particularly equivocal where despite decades of investigation (3,5,26,27), decisive evidence for a causal role of sexually-antagonistic loci on recombination arrest, is conspicuously lacking. The second step is difficult to reconcile with the observation of small degenerated strata (5), within which selective interference should be minimal. Lastly, the causal ordering of events has also been challenged by observation of the early evolution of partial dosage compensation in young sex-chromosomes (28-32).…”

“…mat. 3): notably the occurrence of strata, including small ones (reviewed by 5), the occurrence of early regulatory changes in young sex-chromosomes (28-32) and the lack of decisive evidence for a causal role of sexually-antagonistic loci on recombination arrest, despite decades of investigation (3,5,26,27 Characteristics of inversions in the absence of regulatory evolution. (A) Cumulated distributions of the marginal fitness of newly arising inversions for different size classes of inversions (the different colors, legend at bottom left; the whole chromosome has size 1 on this scale, the sex-determining locus being located at one end of the chromosome).…”