The sex chromosomes of plants and animals often contain large non-recombining regions due to a stepwise cessation of recombination generating “evolutionary strata” of genetic differentiation. This is the case for example for the XY chromosomes in mammals. The reasons for the extension of recombination suppression beyond sex-determining genes remained however unclear. Sexual antagonism, based on differences between males and females, has long been the prevailing hypothesis. However, decades of research have unearthed little evidence to support this hypothesis. The aims of this project are to assess whether chromosomes involved in sexual compatibility in systems lacking male and female functions can nevertheless display a stepwise suppression of recombination beyond mating-compatibility genes, and to explore hypotheses alternative to sexual antagonism to explain such stepwise extension, both experimentally and theoretically.
This project revealed many cases of evolutionary strata in organisms without sexual antagonism, in multiple distant lineages, by generating and analysing genomic data in fungi. We revealed multiple independent events of recombination suppression in the Microbotryum fungi, causing anther-smut disease, as well as in several distant lineages of Sordariales fungi, found in soil. This shows that other mechanisms than sexual antagonistic are able to generate evolutionary strata.
We showed, by mathematical modeling and simulations, that recombination suppression on sex chromosomes can expand because of evolutionary phenomena linked to the presence of recessive deleterious mutations in genomes. We developped two theoretical models with different mechanisms based on the fact that recessive deleterious mutations are sheltered by permanently heterozygous alleles such as in the Y chromosome or mating-type alleles. We thus developed a new theory of sex chromosome evolution to explain the stepwise extensions of recombination suppression on sex-like chromosomes. We validated two predictions of these models : i) that stepwise recombination suppression around mating-type loci in fungi should only occur in diploid-like lineages, and ii) a a sheltered load exist in mating-type chromosomes.
Leveraging on the dataset of dozens of independent events of recombination suppression in Microbotryum fungi, we have elucidated how fast sex chromosomes degenerate, in terms of accumulation of non-synonymous substitutions, non-optimal codon usage and transposable element accumulation.
This project thus used a combination of different approaches and biological systems to refine and test hypotheses to broaden the theory of sex-related chromosome evolution. The EvolSexChrom project challenges the current theory, opening up new avenues of research and creating a paradigm shift in the dynamic research field focusing on the evolution of sex-related chromosomes, relevant to diverse traits and organisms. Because degeneration of the non-recombining chromosomes can impact health and fertility, this can have medical and societal relevance beyond academic importance.
