The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing

Abstract

Large regions of suppressed recombination having extended with time occur in many organisms around genes involved in mating compatibility (sex-determining or mating-type genes). The sheltering of deleterious alleles has been proposed to be involved in such expansions. However, the dynamics of deleterious mutations partially linked to genes involved in mating compatibility are not well understood, especially in finite populations. In particular, under what conditions deleterious mutations are likely to be maintained for long enough near mating-compatibility genes remains to be evaluated, especially under selfing, which generally increases the purging rate of deleterious mutations. Using a branching process approximation, we studied the fate of a new deleterious or overdominant mutation in a diploid population, considering a locus carrying two permanently heterozygous mating-type alleles, and a partially linked locus at which the mutation appears. We obtained analytical and numerical results on the probability and purging time of the new mutation. We investigated the impact of recombination between the two loci and of the mating system (outcrossing, intra and inter-tetrad selfing) on the maintenance of the mutation. We found that the presence of a mating-type locus always sheltered the mutation under selfing, i.e. it decreased the purging probability and increased the purging time of the mutations. The sheltering effect was higher in case of automixis (intra-tetrad selfing). This may contribute to explain why evolutionary strata of recombination suppression near the mating-type locus are found mostly in automictic (pseudo-homothallic) fungi. We also showed that rare events of deleterious mutation maintenance during strikingly long evolutionary times could occur, suggesting that deleterious mutations can indeed accumulate near the mating-type locus over evolutionary time scales. In conclusion, our results show that, although selfing purges deleterious mutations, these mutations can be maintained for very long times near a mating-type locus, which may contribute to promote the evolution of recombination suppression in sex-related chromosomes.

Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi

“…The more often that deleterious mutations segregate in genomes then the more this effect can act: a given fragment evolving recombination cessation and capturing a permanently heterozygous allele will have a greater chance of having a higher fitness differential with the average locus if the distribution of the number of deleterious mutations in this fragment is wider in the population, resulting in stronger selection (Jay et al ., 2022). We found that TEs did not accumulate preferentially in the margin of the non-recombining regions, in contrast to our prediction based on a recent theoretical model showing that, in automictic species such as Microbotryum fungi, a mating-type locus can shelter deleterious mutations in its flanking regions (Tezenas et al ., 2022). As TE insertions can be deleterious, one may have expected that selfing would have promoted their purge more easily farther away from the mating-type locus (Tezenas et al ., 2022).…”

“…We found that TEs did not accumulate preferentially in the margin of the non-recombining regions, in contrast to our prediction based on a recent theoretical model showing that, in automictic species such as Microbotryum fungi, a mating-type locus can shelter deleterious mutations in its flanking regions (Tezenas et al ., 2022). As TE insertions can be deleterious, one may have expected that selfing would have promoted their purge more easily farther away from the mating-type locus (Tezenas et al ., 2022). Not all TE insertions are however deleterious and their active spread may counteract the purging effect.…”

“…The segregation of deleterious mutations near non-recombining regions can foster the expansion of recombination suppression. For example, inversions carrying fewer deleterious mutations than average are selected when rare but suffer from their exposed genetic load when frequent enough to occur as homozygotes; if such less-loaded inversions occur near a permanently heterozygous allele, such as near mating-type loci or Y-like sex-determining alleles, they remain heterozygous and can reach maximal frequencies, thereby expanding the non-recombining region (Jay et al ., 2022; Tezenas et al ., 2022). TEs can themselves promote inversions at the margin of non-recombining regions (Ironside, 2010; Zhang et al ., 2011).…”

“…undergoing intra-tetrad selfing (Hartmann et al ., 2020; Vittorelli et al ., 2022). Theoretical models have suggested that this may be because automictic fungi are dikaryotic for most of their lifecycle, even in ascomycetes, thus allowing the sheltering of deleterious alleles (Jay et al ., 2022), and because automixis can prevent diploid selfing to purge deleterious mutations near mating-type loci (Antonovics & Abrams, 2004; Tezenas et al ., 2022). When non-recombining regions occur on fungal mating-type chromosomes, they are relatively young and some genera display multiple independent events of recombination cessation across closely related species, allowing to study the early stages of genomic degenerescence with independent data points (Carpentier et al ., 2022).…”

Long-term balancing selection and the genetic load linked to the self-incompatibility locus inArabidopsis halleriandA. lyrata

“…Deterministic models by Strobeck (1980) and Leach et al (1986) showed that even lethal mutations can be effectively sheltered, provided they are tightly linked to strongly balanced allelic lines. More recently, Tezenas et al (2022) observed that linkage to a mating-type locus, such as found in some fungi (where typically two strongly balanced allelic lines segregate), decreases the probability and increases the time for purging of linked deleterious mutations. Stochastic simulations by Llaurens et al (2009) further predicted that the sheltering of deleterious recessive mutations should be related to the number of balanced allelic lines, with higher probabilities of fixation of deleterious alleles within an allelic line when the number of alleles increases.…”