Mating Compatibility and Degeneration of Non-Recombining Chromosomes - SUMMARY / ABSTRACT
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.
