Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Abstract

Summary Genomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self‐incompatibility loci and fungal mating‐type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating‐type loci in fungi, sometimes encompassing vast regions of the mating‐type chromosomes. The suppression of recombination at mating‐type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating‐type genes in fungi (‘evolutionary strata’), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating‐type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.

Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex

“…2008 ; Branco et al. 2018 ; Hartmann et al. 2020 ), although this phenomenon has been much less studied than in plant and animal sex chromosomes.…”

“…2008 ; Branco et al. 2017 , 2018 ; Hartmann et al. 2020 ), indicating a stepwise extension of the recombination suppression away from the mating-type loci.…”

Modeling the stepwise extension of recombination suppression on sex chromosomes and other supergenes through deleterious mutation sheltering

“…These structures are defined by extensive regions of recombination suppression encompassing multiple genes, and they control iconic polymorphisms, such as sexual dimorphism or color polymorphism, in many organisms, including humans [1][2][3][4][5] . Supergenes, and sex chromosomes in particular, often display a stepwise extension of non-recombining regions, generating "evolutionary strata" of differentiation 4,[6][7][8][9][10] . It is generally thought that the regions of recombination suppression on sex chromosomes gradually expand because selection favors the linkage of sex-determining genes to sexually antagonistic loci (i.e.…”

“…16). More critically, the gradual expansion of recombination suppression has been observed around many fungal mating-type loci, despite the lack of male or female functions and hence of sexual antagonism in these species 8,17 , as well as around other supergenes 9,10 . Alternative explanations for the evolution of non-recombining sex chromosomes have been proposed, such as meiotic drive 18 and genetic drift 19 , but these models are also subject to similar limitations: they apply only in specific conditions and are poorly supported by empirical data.…”

“…In plants, for example, selection at the haploid stage seems to result in the efficient purging of recessive deleterious mutations 46 , potentially accounting for the smaller non-recombining region observed on the sex chromosomes of plants and algae than on those of animals 47,48 . In fungi, evolutionary strata around mating-type genes have been reported only in species with an extended dikaryotic stage, and not those with only a haploid phase 8 . This is consistent with our model, in which the stepwise recombination suppression evolves through the sheltering of deleterious mutations, which cannot occur in haploid organisms.…”