Periodic Reporting for period 3 - EvolSexChrom (Testing new hypotheses on the evolution of sex-related chromosomes)
Reporting period: 2022-10-01 to 2024-03-31
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. The reasons for the extension of recombination suppression beyond sex-determining genes remain unclear. Sexual antagonism, involving the linkage to sex-determining genes of alleles beneficial in only one sex, has long been the prevailing hypothesis, as this explanation is both theoretically plausible and attractive. 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, both experimentally and theoretically.
We found many cases of evolutionary strata in organisms without sexual antagonism, by generating and analysing genomic data (in fungi and oomycetes) and by a review of the literature ; we showed that there other types of antagonistic selection were unlikely to occur in these organisms. This shows that other mechanisms than sexual antagonistic are able to generate evolutionary strata.
We showed, by mathematical modeling and stochastic simulations, that recombination suppression on sex chromosomes and around supergenes can expand under a wide range of parameter values simply because it shelters recessive deleterious mutations, which are ubiquitous in genomes. Permanently heterozygous alleles, such as the male-determining allele in XY systems or fungal mating-type chromosomes, protect linked chromosomal inversions against the expression of their recessive mutation load, leading to the successive accumulation of inversions around these alleles without antagonistic selection. We therefore developed a new theory of sex chromosome evolution, showing that a simple and testable hypothesis can explain the stepwise extensions of recombination suppression on sex chromosomes, mating-type chromosomes and supergenes in general. We are analyzing genomic data to test the predictions of our model and we developed an innovative experimental evolution approach with functional manipulations to assess the ability of the proposed mechanisms to generate evolutionary strata.
This project thus uses a synergic 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.
We found many cases of evolutionary strata in organisms without sexual antagonism, by generating and analysing genomic data (in fungi and oomycetes) and by a review of the literature ; we showed that there other types of antagonistic selection were unlikely to occur in these organisms. This shows that other mechanisms than sexual antagonistic are able to generate evolutionary strata.
We showed, by mathematical modeling and stochastic simulations, that recombination suppression on sex chromosomes and around supergenes can expand under a wide range of parameter values simply because it shelters recessive deleterious mutations, which are ubiquitous in genomes. Permanently heterozygous alleles, such as the male-determining allele in XY systems or fungal mating-type chromosomes, protect linked chromosomal inversions against the expression of their recessive mutation load, leading to the successive accumulation of inversions around these alleles without antagonistic selection. We therefore developed a new theory of sex chromosome evolution, showing that a simple and testable hypothesis can explain the stepwise extensions of recombination suppression on sex chromosomes, mating-type chromosomes and supergenes in general. We are analyzing genomic data to test the predictions of our model and we developed an innovative experimental evolution approach with functional manipulations to assess the ability of the proposed mechanisms to generate evolutionary strata.
This project thus uses a synergic 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.
We have confirmed using gene expression data that evolutionary strata evolved in the fungus Microbotryum lychnidis-dioicae without antagonistic selection. Using new high-quality genome assemblies, we have revealed new independent events of recombination suppression across the Microbotryum genus and further instances of stepwise recombination suppression. Leveraging on this dataset of 21 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. Using available genomic data, we have confirmed that evolutionary strata have evolved in several fungi in which this was suspected but not formally demonstrated. We have written an invited review showing that stepwise evolution of recombination suppression is prevalent around mating-type genes in fungi, and we have reviewed the possible evolutionary and proximal causes. We have generated and analysed genomic data showing that the size of the non-recombining region around the mating-type locus was variable within and among species in the fungal Podospora genus. We have generated and analysed genomic data showing that a very large non-recombining region was present around the mating-type locus in the oomycete Plasmopara viticola, causing the downy mildiew disease on grapes. We have revealed stepwise recombination suppression around the mating-type locus in multiple fungi (Agaricus bisporus, Podospora pseudo-comata, Schizothecium tetrasporum, Cryphonectria parasitica). We have developped a theoretical model that shows that recombination suppression can extend stepwise around a permanently heterozygous allele for sheltering deleterious mutations ; the model has generated predictions to be tested using genomic data. We have generated the mutants for the experimental evolution experiment, that is under way, to check whether evolutionary strata can evolve for sheltering deleterious mutations. Our work has let so far to 13 scientific publications, including in highly accessed journals (PLoS Biology, Current Biology, Molecular Biology and Evolution, Nature Communications) and we have organized in June 2022 an international conference gathering the 16 most reknown worldwide experts on sex chromosomes and supergenes. We have performed a short outreach movie on the project: https://www.youtube.com/watch?v=YNF2023Zx3Q(opens in new window)
In this project, we have generated a new theory for the evolution of sex chromosomes. We have shown that other mechanisms than sexual antagonism are able to generate evolutionary strata on sex chromosomes, using genomic data and theoretical modeling. We have generated predictions to test our model. Our work has been very well received by the community and several teams want to test our predictions on their favourite model organisms. We will also use comparative and population genomic approaches to test predictions, and an innovative experimental evolution approach with functional manipulations is under way to assess the ability of the proposed mechanisms to generate evolutionary strata. 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.