Sheltered load in fungal mating-type chromosomes revealed by fitness experiments

Sex chromosomes and mating-type chromosomes can carry large regions with
suppressed recombination. As a result of a lower efficacy of selection,
recessive deleterious mutations are expected to accumulate in these
non-recombining regions. 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 three
Sordariales species, 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 for Podospora anserina at
18°C and for Schizothecium tetrasporum and Schizothecium tritetrasporum at
22°C under light. These findings suggest the presence of a sheltered load,
i.e., recessive deleterious mutations at the heterozygous state in or near
non-recombining regions, associated to a specific mating-type allele.
Genomic analyses indeed suggested that the non-recombining regions around
the mating-type locus likely carries heterozygous deleterious mutations,
while the rest of the genome was mostly homozygous. We also showed that
the difference in growth rates did not result from different numbers or
densities of nuclei between homokaryons and heterokaryons. Leveraging 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.