Sex chromosomes as supergenes of speciation: why amphibians defy the rules?

Abstract

As reflected by the two rules of speciation (Haldane's rule and the large X-/Z-effect), sex chromosomes are expected to behave like supergenes of speciation: they recombine only in one sex (XX females or ZZ males), supposedly recruit sexually antagonistic genes and evolve faster than autosomes, which can all contribute to pre-zygotic and post-zygotic isolation. While this has been mainly studied in organisms with conserved sex-determining systems and highly differentiated (heteromorphic) sex chromosomes like mammals, birds and some insects, these expectations are less clear in organismal groups where sex chromosomes repeatedly change and remain mostly homomorphic, like amphibians. In this article, we review the proposed roles of sex-linked genes in isolating nascent lineages throughout the speciation continuum and discuss their support in amphibians given current knowledge of sex chromosome evolution and speciation modes. Given their frequent recombination and lack of differentiation, we argue that amphibian sex chromosomes are not expected to become supergenes of speciation, which is reflected by the rarity of empirical studies consistent with a ‘large sex chromosome effect’ in frogs and toads. The diversity of sex chromosome systems in amphibians has a high potential to disentangle the evolutionary mechanisms responsible for the emergence of sex-linked speciation genes in other organisms. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

Searching for signatures of sexually antagonistic selection on stickleback sex chromosomes

“…This possibility is supported by examples of male-beneficial genes that have been transposed from autosomes to the SDR of the sex chromosomes of Drosophila [ 16 – 21 ], mammals [ 22 , 23 ], and the threespine stickleback [ 24 ]. The second alternative hypothesis is even simpler—some sex chromosomes may simply never accrue loci under SAS in a fashion disproportionate to the rest of the genome [ 25 ]. Indeed, recent work has demonstrated that population genetic approaches may be biased to identifying SAS on the X [ 26 ], and there have been several calls to search for alternative explanations for the evolution of sex chromosomes in general [ 27 , 28 ].…”

Genomic architecture of supergenes: connecting form and function

“…Not all supergenes show suppressed recombination between haplotypes. Dufresnes et al [ 37 ] investigate sex chromosomes that lack recombination suppression in the heterogametic sex. In most species, archetypal sex chromosomes come in two differentiated versions that do not recombine over a large stretch in the heterogametic sex (the male in XY systems such as mammals or the female in WZ systems such as birds).…”

“…Dufresnes et al . [ 37 ] review this amphibian defiance of the classical laws of sex chromosome evolution and examine what it can teach us about the role of sex chromosomes as supergenes of speciation. The generally homomorphic sex chromosomes of amphibians do not appear to play a disproportionally large role in reproductive isolation as compared to the autosomes.…”

“…Dufresnes et al . [ 37 ] highlight amphibians as a promising model to contrast with systems where sex chromosomes act as supergenes of speciation.…”

B Chromosomes in Psalidodon scabripinnis (Characiformes, Characidae) Species Complex

“…Keeping in mind that the B chromosomes have large blocks of genome duplications and several kinds of selfish DNA, they are probable spots for these new interactions. As sex chromosomes that evolve faster than autosomes [ 95 ], B chromosome evolution and interactions with A genomes can rapidly create incompatibilities between two isolated subpopulations.…”