Slower-X: reduced efficiency of selection in the early stages of X chromosome evolution

Abstract

Differentiated X chromosomes are expected to have higher rates of adaptive divergence than autosomes, if new beneficial mutations are recessive (the “faster-X effect”), largely because these mutations are immediately exposed to selection in males. The evolution of X chromosomes after they stop recombining in males, but before they become hemizygous, has not been well explored theoretically. We use the diffusion approximation to infer substitution rates of beneficial and deleterious mutations under such a scenario. Our results show that selection is less efficient on diploid X loci than on autosomal and hemizygous X loci under a wide range of parameters. This “slower-X” effect is stronger for genes affecting primarily (or only) male fitness, and for sexually antagonistic genes. These unusual dynamics suggest that some of the peculiar features of X chromosomes, such as the differential accumulation of genes with sex-specific functions, may start arising earlier than previously appreciated.

Phased assembly of neo-sex chromosomes reveals extensive Y degeneration and rapid genome evolution inRumex hastatulus

“…In contrast, we see no sign of excess gene loss on the old X-linked region (Table S6, Figure 5A), providing no evidence of early gene loss on the X chromosome, as found recently in other systems (Mrnjavac et al 2023). Furthermore, there is no sign of excess gene loss in the ‘new’ sex-linked region (NeoY), suggesting a lack of rapid deletion of Y-linked genes since the chromosomal fusion.…”

Sex chromosome heteromorphism and the Fast‐X effect in poeciliids

“…This does not necessarily require male hemizygosity (Presgraves & Orr, 1998), just recombination suppression between the X and Y chromosomes. In the absence of recombination, young homomorphic sex chromosomes may additionally experience a Fast‐X effect as recessive deleterious mutations accumulate on X‐linked loci due to sheltering by the functional gene copies on the Y chromosome (Mrnjavac et al, 2023).…”

“…Notably, all the cases of Fast‐X above were observed in highly heteromorphic sex chromosomes, where very few genes, if any, remain on the Y chromosome and the X is largely hemizygous in the heterogametic sex. As such, it remains unclear how early in the process of sex chromosome differentiation the Fast‐X effect becomes detectible, and how important Y degeneration is in X chromosome evolution (Mrnjavac et al, 2023; Presgraves & Orr, 1998).…”

“…This non-adaptive cause of Fast-X does not necessarily require male hemizygosity, just recombination suppression between the X and Y chromosomes and differences in effective population size between X-linked and autosomal loci, and could apply to X loci where the Y copy is expressed and remains functional. The non-adaptive causes of Fast-X might actually be exacerbated in systems that lack male hemizygosity, as recent theoretical work predicts that in the absence of recombination, recessive deleterious mutations in males can accumulate on young X-linked genes as they become sheltered by the remaining functional Y chromosome gene copies (Mrnjavac et al, 2023).…”

“…The signature of Fast-X at internal branches of the phylogeny can be used to date the origin of Y degeneration. If the sex chromosome arose recently in the immediate ancestor of the clade, we might expect Fast-X to be confined to P. picta and P. parae and internal branches connecting these two species, with Fast-X patterns in P. reticulata and P. wingei less pronounced or absent, consistent with their far reduced levels of male hemizygosity (Mrnjavac et al, 2023). In contrast, if the sex chromosomes arose much earlier, we might expect Fast-X patterns, evolving over long periods of time in the distant ancestor of the clade, to be evident in internal branches of the phylogeny.…”