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Recombination suppression often evolves in sex chromosomes and around mating-type loci. In the invasive chestnut blight fungus Cryphonectria parasitica (Ascomycota), a genomic region was previously suggested to lack recombination and to be partially linked to the mating-type (MAT) locus based on the analysis of a few progenies. Using hundreds of available C. parasitica genomes and generating several new high-quality genome assemblies from the native and introduced range of the pathogen, we show that a ca. 1.2 Mb genomic region proximal to the mating-type locus lacks recombination worldwide, thus constituting a supergene. In invasive populations with extensive local genomic data and a recombining genome-wide structure, this MAT-proximal region displayed two highly differentiated haplotypes, that were strongly associated to mating types, but not completely, and with footprints of selective sweeps. High-quality assemblies of the two haplotypes in invasive and native populations revealed an inversion in one of the two MAT-proximal haplotypes and footprints of degeneration worldwide, the MAT-proximal region being enriched in gene disruptions, non-synonymous substitutions and transposable elements in both haplotypes. The divergence between the two haplotypes in the supergene was estimated to have occurred at least 1.5 million years ago and two haplotypes segregate in all continents, including the native range. Footprints of selective sweep, high differentiation between haplotypes, their occurrence on different continents, their balanced frequencies within populations, their genomic rearrangements and degeneration worldwide, altogether suggest an ancient recombination suppression maintained by selection. This study sheds light on an interesting case of a large supergene partially linked to a mating compatibility locus, and on balancing selection maintaining differentiated haplotypes, possibly involving deleterious mutations and/or host adaptation in a devastating tree pathogen.
Recombination suppression often evolves in sex chromosomes and around mating-type loci. In the invasive chestnut blight fungus Cryphonectria parasitica (Ascomycota), a genomic region was previously suggested to lack recombination and to be partially linked to the mating-type (MAT) locus based on the analysis of a few progenies. Using hundreds of available C. parasitica genomes and generating several new high-quality genome assemblies from the native and introduced range of the pathogen, we show that a ca. 1.2 Mb genomic region proximal to the mating-type locus lacks recombination worldwide, thus constituting a supergene. In invasive populations with extensive local genomic data and a recombining genome-wide structure, this MAT-proximal region displayed two highly differentiated haplotypes, that were strongly associated to mating types, but not completely, and with footprints of selective sweeps. High-quality assemblies of the two haplotypes in invasive and native populations revealed an inversion in one of the two MAT-proximal haplotypes and footprints of degeneration worldwide, the MAT-proximal region being enriched in gene disruptions, non-synonymous substitutions and transposable elements in both haplotypes. The divergence between the two haplotypes in the supergene was estimated to have occurred at least 1.5 million years ago and two haplotypes segregate in all continents, including the native range. Footprints of selective sweep, high differentiation between haplotypes, their occurrence on different continents, their balanced frequencies within populations, their genomic rearrangements and degeneration worldwide, altogether suggest an ancient recombination suppression maintained by selection. This study sheds light on an interesting case of a large supergene partially linked to a mating compatibility locus, and on balancing selection maintaining differentiated haplotypes, possibly involving deleterious mutations and/or host adaptation in a devastating tree pathogen.
Sex-linked and autosomal loci experience different selective pressures and evolutionary dynamics. X (or Z) chromosomes are often hemizygous, as Y (or W) chromosomes often degenerate. Such hemizygous regions can be under greater efficacy of selection, as recessive mutations are immediately exposed to selection in the heterogametic sex (the so-called Faster-X or Faster-Z effect). However, in young non-recombining regions, Y/W chromosomes often have many functional genes, and many X/Z-linked loci are therefore diploid. The sheltering of recessive mutations on the X/Z by the Y/W homolog is expected to drive a Slower-X (Slower-Z) effect for diploid X/Z loci, i.e. a reduction in the efficacy of selection. While the Faster-X effect has been studied extensively, much less is known empirically about the evolutionary dynamics of diploid X or Z chromosomes. Here, we took advantage of published population genomic data in the female-heterogametic human parasiteSchistosoma japonicumto characterize the gene content and diversity levels of the diploid and hemizygous regions of the Z chromosome. We used different metrics of selective pressures acting on genes to test for differences in the efficacy of selection in hemizygous and diploid Z regions, relative to autosomes. We found consistent patterns suggesting reduced Ne, and reduced efficacy of purifying selection, on both hemizygous and diploid Z regions. Moreover, relaxed selection was particularly pronounced for female-biased genes on the diploid Z, as predicted by Slower-Z theory.
Sex chromosomes and mating-type chromosomes can carry large regions with suppressed recombination. In these non-recombining regions, recessive deleterious mutations are expected to occur, as i) they are predicted to accumulate as a result of lower efficacy of selection, and ii) they may even pre-exist and drive the evolution of recombination suppression. Multiple genomic analyses have indirectly inferred the presence of deleterious mutations in sex and mating-type chromosomes, but direct experimental evidence remains scarce. Here, we performed fitness assays in fungi with megabase-large and young non-recombining regions around the mating-type locus, using theSchizothecium tetrasporumandPodospora anserinaspecies complexes, to test whether heterokaryons (diploid-like, heterozygous at the mating-type locus) exhibited a fitness advantage over homokaryons (haploid-like, with a single mating-type allele), in terms of spore germination dynamics or mycelium growth speed, under different conditions of light and temperature. We found a faster growth of heterokaryons compared to one of the homokaryons forP. anserinaat 18°C, forS. tetrasporumandS. tritetrasporumat 22°C under light, and also at 22°C in the dark forS. tetrasporum. These findings suggest the presence of a sheltered load, i.e. recessive deleterious mutations at the heterozygous state in or near non-recombining regions, as these species are highly homozygous otherwise. Leveraging on the experimental assets of fungi, allowing cultivating separately haploid-like and diploid-like life stages, our experiments provided one of the rare direct experimental evidence of sheltered load around mating-compatibility loci, which is crucial for our understanding of sex-related chromosome evolution.
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