Genes in linkage with determinants of reproductive compatibility are subject to mutational degeneration, but the processes by which suppressed recombination expands on such chromosomes and the temporal dynamics of mutational decay are not well established in empirical studies. These dynamics of chromosomal evolution are important because of their impacts on mutation accumulation, the emergence of sex-linked disorders, and individual fitness and adaptive potential. Contributing to the long-term goal of understanding how changes in genome architecture can feedback to cause genetic decay, the proposed work would utilize resources in a genus of fungal pathogens as a useful empirical model. Reproductive compatibility in these fungi helps to isolate meiotic recombination for studying its role in driving changes in genetic integrity. With phylogenetic comparative methods, the proposed work will test the following principles or predictions: 1) that the evolutionary history of recombination suppression around reproductive compatibility loci is one of staged expansion, with the formation of ?strata? of differentiation between chromosomes in the homologous pair; 2) the theoretical prediction that gene degeneration (mutational decay and hemizygous gene losses) accrues rapidly following cessation of recombination but decelerates over time; and 3) that the restoration of co-linearity and meiotic recombination involves the permanent fixation of degenerate genes in a homozygous state, presenting fitness challenges that have been predicted to restrict sex chromosomes to an irreversible ?end-point? of their degenerate evolution. Regarding the first two of these specific aims, phylogenetic comparative methods will include two dozen species of the fungal genus Microbotryum, representing a diversity of chromosomal architecture, with most genomes already in progress for assembly by PacBio sequencing and restriction-digest optical maps.
The third aim will utilize the discovery of an evolutionary reversion, which broke linkage relationships with the mating compatibility genes and restored co-linearity to the chromosome pair. This is a novel opportunity to test principles of sex chromosome evolution with an autosome-like derived condition. While the methods are well established and allow for the direct involvement of undergraduate students in multiple specified components, the approach is highly innovative because it tests hypotheses on genetic degeneration that constitute established theory, but for which other organisms have been intractable for large-scale comparative studies needed to obtain empirical support. The project is expected to reveal the progress of genetic degeneration that contributes to mutational decay and gene loss in non-recombining chromosomes, which are significant and wide-spread features from humans, to plants and fungi, including many eukaryotic pathogens. This AREA project would contribute to the mentoring of multiple undergraduates through active participation in research. Moreover, the project would greatly enrich the vitality of life sciences on the liberal arts campus.
This research is relevant to public health because the genes on non-recombining sex chromosomes have a central role in determining reproductive traits and many other aspects of development and fitness, but they are also especially prone to genetic degeneration and the emergence of sex-linked mutational disorders. Knowledge about the tempo of mutational decay once genes become linked to reproductive compatibility is not currently based upon strong empirical support, and the use of a fungal model provides the tractability to test existing theoretical predictions about integrity of genes under suppressed recombination, while eliminating the effects of other confounding evolutionary factors. More broadly, regions linked to reproductive compatibility are also known to include genes important to variation in pathogenicity and virulence in fungal pathogens where the proposed studies will increase understanding their long-term evolutionary dynamics.
| Branco, Sara; Carpentier, Fantin; Rodríguez de la Vega, Ricardo C et al. (2018) Multiple convergent supergene evolution events in mating-type chromosomes. Nat Commun 9:2000 |
| Branco, Sara; Badouin, Hélène; Rodríguez de la Vega, Ricardo C et al. (2017) Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism. Proc Natl Acad Sci U S A 114:7067-7072 |
| Coelho, Marco A; Bakkeren, Guus; Sun, Sheng et al. (2017) Fungal Sex: The Basidiomycota. Microbiol Spectr 5: |
