Population genomics of degenerative genome evolution

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One of the most striking features of genome evolution is found in cases of degenerative evolution, whereby large regions of the genome experience gene silencing and loss. Such genome degeneration is surprising, as it runs counter to the general prediction that natural selection should continually be driving genes towards improved function. Despite this, large-scale gene degeneration has occurred repeatedly, including recurrent degeneration of genes on non-recombining sex chromosomes, and loss of duplicate genes following whole genome duplication. The evolutionary forces driving degenerative evolution remain unclear; one possibility is that it may be driven by a 'passive' process of gene inactivation and loss through a reduction in the efficacy of natural selection. While reduced selection is likely important, the process of adaptation may also contribute: differences in fitness between derived gene copies may lead to adaptive gene inactivation and loss, accelerating degeneration. ***In this proposal, my lab will examine several systems experiencing recent transitions that enable tests of the forces driving degenerative evolution. First, we will examine genome evolution in a recently derived species that experienced whole genome duplication (polyploidy), Capsella bursa-pastoris. We will investigate the early dynamics of adaptation and genome evolution following whole genome duplication, to test whether genes experiencing degeneration and silencing are subject to higher rates of adaptive evolution. We will also test whether the past evolutionary history of parental species influences gene silencing and loss in a recent polyploid. Second, we will use comparative genome and RNA sequencing to identify sex-linked genes across the plant genus Rumex, which has 'young' sex chromosomes; this will allow us to quantify the extent of gene degeneration and recombination suppression, and ask whether adaptive evolution on the X chromosome accelerates gene silencing and loss on the Y. This comparative approach should enable unique insights into the factors driving differential rates of degenerative evolution across species. Finally, effective loss of sexual reproduction has occurred numerous times in the evening primrose genus Oenothera. We will conduct comparative genomics in this system to investigate the extent to which these asexual lineages experience gene degeneration and loss. We will also investigate whether gene degeneration in an asexual lineage is halted by the expression of genes in the haploid pollen phase, where deleterious and beneficial mutations become exposed to selection. Overall, these studies of degenerative evolution will help provide new insights into the joint and unique effects of ploidy (gene copy number) and loss of recombination in driving the efficacy of natural selection, and the role of adaptive evolution in gene silencing and loss.**