Demography and Mating System Shape the Genome-Wide Impact of Natural Selection in Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation, and can affect the impact of natural selection. However, while theory has shown that low levels of outcrossing may be sufficient to stop accumulation of deleterious alleles, few empirical studies have addressed this directly.

We analyzed whole genome resequencing data from 41 A. alpina individuals to study the effects of variation in outcrossing rates on purifying selection. We found that A. alpina showed strong population structure, and levels of genetic diversity varied greatly across populations, with the highest levels of genetic diversity found in an outcrossing population from Greece. In agreement with expectations from theory, populations with a low level (~20%) of outcrossing maintained genetic diversity and did not experience relaxed purifying selection. In contrast, highly selfing populations from Sweden had extremely low levels of genetic diversity, and appear to have gone through a very severe bottleneck, the timing of which is consistent with post-glacial recolonization. Highly selfing populations exhibited evidence for elevated genetic load, including fixation of major-effect deleterious mutations. Using forward population genetic simulations, we showed that selfing alone cannot explain this result, and that demography is also important.

In conclusion, our results empirically confirm that a low level of outcrossing is sufficient to prevent loss of diversity and accumulation of deleterious mutations. Our results further demonstrate that understanding the combined impact of demography and mating system on selection is of great importance in the context of past and current climate change.