Another part of research in progress in the team relates to the study of the adaptive causes underlying the striking evolution of sex chromosomes, by again using fungi as useful eukaryotic models. The sex chromosomes in plants and animals often show recombination suppression (for example between X and Y in humans), which leads to differentiation and degeneration; for example, the Y chromosome is very small in humans, with very few genes and many repeated sequences. The current dominant theory to explain the suppression of recombination between the sex chromosomes in plants and animals, which often occurred in several successive steps (called evolutionary strata), is the existence of traits which are beneficial in males but deleterious in females, or conversely. There would then exist a selection to successively link the genes responsible for these traits to the sex-determinism genes. However, very little evidence of this process could be documented despite years of research. The fungi provide, here again, good models to test these hypotheses, because some have mating-type chromosomes with recombination suppression, whereas the mating types are not related to male and female functions. In fungi, the genes determining mating types control sexual compatibility, two haploid genotypes being compatible if, and only if, they have different alleles that mating-type genes, but without other different traits between the mating types.

The Microbotryum fungi were the first ones in which mating types were identified, at the beginning of the 20th century, and the first on which dimorphic mating-type chromosomes with suppressed recombination were described. For a long time, these chromosomes could not be assembled given their high quantity of repeated sequences. Thanks to the complete assembly of the M. lychnidisdioicae genome that we have just obtained, we could show that the mating-type chromosomes are non-recombining across nearly 90% their length. Moreover, they present an exceptional degree of rearrangements and degeneration. Hundreds of genes were lost in one or the other mating type, and many deleterious changes were identified, in terms of replacement of amino-acids, sub-optimal gene expression or accumulation of transposable elements. Even more remarkably, we detected evolutionary strata on the mating-type chromosomes of M. lychnidisdioicae, whereas there exist no male or female function in these fungi, all gametes displaying the same size. The mating-type chromosomes of M. lychnidisdioicae thus present remarkable convergence with the sex chromosomes of plants and animals, despite lack of association with male and female functions. These results suggest that the dominant evolutionary theory explaining the evolution of sex chromosomes by differential optimal adaptation of males and females should be reconsidered. We are testing alternative hypotheses, such as a selection to shelter in a permanent heterozygous state the deleterious mutations which would accumulate in edges of the non-recombining regions. In addition, the unique material of extremely well assembled genomes of several Microbotryum species enabled us to show that the suppression of recombination has evolved many times independently and recently, by different chromosomal rearrangements, and with independent evolutionary strata. This is thus a case of remarkable evolutionary convergence, with likely a strong adaptive advantage, which we are trying to identify.