Can mechanistic constraints on recombination reestablishment explain the long-term maintenance of degenerate sex chromosomes?

Abstract

Y and W chromosomes often stop recombining and degenerate. Different theories have been proposed to explain these observations. The classic theory supposes that recombination arrest is favored because it allows to permanently link sex-antagonistic alleles to the sex in which they are favorable. The regulatory theory supposes that recombination arrest is initially caused by lucky inversions on the Y or W carrying fewer deleterious mutations than average, which then become selectively stabilized by the evolution of nascent dosage compensation creating sex-antagonistic regulatory effects. Last, the shelter theory also supposes that lucky Y (or W) inversions do occur, but that they are maintained in the long term because of a lack of genetic variation to restore recombination. The last two theories are comparable in the sense that they do not require sexually dimorphic traits, and are based primarily on the flux of deleterious mutations. In this paper, we focus on the shelter theory and show that contrarily to previous claims, it can hardly explain the evolution of sex chromosomes. We show that it is not robust to extremely low rates of recombination restoration, that it would cause population extinction rather than Y degeneration, and that it is orders of magnitudes less efficient than the mechanism described in the regulatory theory. We also argue that the assumption of a lack of genetic variation to restore recombination is unplausible given known mechanisms of recombination variation, and given the extremely small rates of restoration that are sufficient to make the shelter theory inoperant.

A single theory for the evolution of sex chromosomes and the two rules of speciation

“…We recently proposed a new theory for the evolution of non-recombining, degenerated, and dosagecompensated sex chromosomes based on XY regulatory divergence and the early emergence of dosage compensation (DC) [34][35][36] . We show here that the same theory also predicts Haldane's rule and the large X effect.…”

Do deleterious mutations promote the evolution of recombination suppression between X and Y chromosomes?

“…While a large body of population genetics research focuses on the role of sex differences in selection during the evolution of recombination supression between sex chromosomes [1,2], several recent theoretical studies have directed attention to alternative hypotheses [3][4][5]. Among these alternatives is what has been called "the sheltering hypothesis" for recombination suppression between sex chromosomes [4,6,7].…”

“…If this probability is greater than the value for a selectively neutral mutation, there is a net selective advantage to the inversion. The fixation probability can be found either by analytical models that assume that mutations are sufficiently strongly selected against that their behaviour can be treated deterministically (i.e., N s ≫ 1; [4,5,10], or by computer simulations of more general situations in which genetic drift as well as selection and mutation is important [3,6,7]).…”