Hill-Robertson Interference Reduces Genetic Diversity on a Young Plant Y-Chromosome

X and Y chromosomes differ in effective population size (Ne), rates of recombination, and exposure to natural selection, all of which can affect patterns of genetic diversity. On Y chromosomes with suppressed recombination, natural selection is expected to eliminate linked neutral variation, and lower the Ne of Y compared to X chromosomes or autosomes. However, female-biased sex ratios and high variance in male reproductive success can also reduce Y-linked Ne, making it difficult to infer the causes of low Y-diversity. Here, we investigate the factors affecting levels of polymorphism during sex chromosome evolution in the dioecious plant Rumex hastatulus (Polygonaceae). Strikingly, we find that neutral diversity for genes on the Y chromosome is, on average, 2.1% of the value for their X-linked homologs, corresponding to a chromosome-wide reduction of 93% compared to the standard neutral expectation. We demonstrate that the magnitude of this diversity loss is inconsistent with reduced male Ne caused by neutral processes. Instead, using forward simulations and estimates of the distribution of deleterious fitness effects, we show that Y chromosome diversity loss can be explained by purifying selection acting in aggregate over a large number of genetically linked sites. Simulations also suggest that our observed level of Y-diversity is consistent with the joint action of purifying and positive selection, but only for models in which there were fewer constrained sites than we empirically estimated. Given the relatively recent origin of R. hastatulus sex chromosomes, our results imply that Y-chromosome degeneration in the early stages may be largely driven by selective interference rather than by neutral genetic drift of silenced Y-linked genes.