Tempo of Degeneration Across Independently Evolved Nonrecombining Regions

Abstract

Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression can evolve and lead to genomic degeneration, in particular on sex chromosomes. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, leveraging on 22 independent events of recombination suppression identified on mating-type chromosomes of anther-smut fungi, including newly identified ones. Using previously available and newly generated high-quality genome assemblies of alternative mating types of 13 Microbotryum species, we estimated degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions compared to autosomes, that was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. The frequency of optimal codons rapidly decreased following recombination suppression and reached an asymptote after ca 3 Mya. The strength of purifying selection remained virtually constant at dN/dS = 0.55, i.e. at an intermediate level between purifying selection and neutral evolution. Accordingly, non-synonymous differences between mating-type chromosomes increased linearly with stratum age, at a rate of 0.015 per MY. We thus develop a method for disentangling effects of reduced selection efficacy from GC-biased gene conversion in the evolution of codon usage and we quantify the tempo of degeneration in non-recombining regions, which is important for our knowledge on genomic evolution and on the maintenance of regions without recombination.

Stepwise recombination suppression around the mating-type locus in the fungusSchizothecium tetrasporum(Ascomycota, Sordariales)

“…More precisely, recombination suppression may be selected because it protects DNA fragments with fewer deleterious mutations than average in the population, but the load of these mutations will still prove problematic when they become frequent enough to become homozygous; the capture of a permanently heterozygous allele prevents this effect (14). This mechanism can also explain the evolution of successive evolutionary strata, as observed here in S. tetrasporum and, previously, in N. tetrasperma and P. pseudocomata (22,27,27,48), the basidiomycete mushroom Agaricus bisporus (53) and repeatedly in Microbotryum basidiomycete fungi, plant pathogens in natural ecosystems (8,9,18,54). This mechanism may also account for the suppression of recombination in N. tetrasperma .…”

“…We found no enrichment in repeats, rearrangements or non-synonymous substitutions, whereas transposable elements, non-synonymous substitutions and non-optimal codon usage have all been found to increase with time since recombination suppression in the mating-type chromosomes of Microbotryum anther-smut fungi (9,54,62). Gene disruptions due to small indels remain to be investigated.…”

Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

“…We found signs of degeneration in the non-recombining region in terms of gene losses and gene disruptions. In contrast, we found no enrichment in repeats, rearrangements or non-synonymous substitutions, whereas transposable elements, non-synonymous substitutions and non-optimal codon usage have all been found to increase with time since recombination suppression in the mating-type chromosomes of Microbotryum anther-smut fungi [9,46,80]. The suppression of recombination may have occurred too recently in S. tetrasporum for these marks of degeneration to evolve or there may be an efficient mechanism of TE control.…”

“…This mechanism can also explain the evolution of successive evolutionary strata, as observed here in S. tetrasporum, and previously in N. tetrasperma and P. pseudocomata [26,31,72], but also in the cultivated variety of the basidiomycete mushroom Agaricus bisporus var. bisporus [50], and repeatedly in Microbotryum basidiomycete fungi, plant pathogens in natural ecosystems [8,9,18,80]. All these lineages undergo mostly or only automixis (intra-tetrad mating) and have only two mating types, which has been theoretically shown to favor the sheltering of deleterious alleles near the mating-type locus [16,47,48].…”

Domestication of different varieties in the cheese-making fungusGeotrichum candidum

“…This was the case even in the clonal Cheese_2 population, while degeneration can be expected to be particularly strong in clonally replicated populations as recombination allows more efficient selection. The absence of sexual reproduction in the Cheese_2 population may be too recent to observe degeneration (Carpentier et al, 2022). We also investigated the presence of premature stop codons due to nonsense mutations in all genes with predicted functions in both CLIB 918 and LMA-244 reference genomes.…”