Whole-genome duplication increases genetic diversity and load in outcrossing Arabidopsis

Genetic variation underpins evolutionary change, but accumulation of slightly deleterious mutations also increases mutation load. There are multiple factors affecting the extent of load such as population size and breeding system, yet other potential determinants remain unexplored. A common macromutation, whole-genome duplication (WGD) occurs broadly across Eukaryotes, yet we lack a clear understanding of how WGD impacts neutral and selective processes within a population. Using forward simulations and empirical analysis of 632 short- and 16 long-read sequenced individuals of Arabidopsis arenosa (23 diploid and 42 natural autotetraploid populations), we test for the effects of WGD on genome-wide diversity and mutation load. Our simulations show how genetic variation gradually rises in autotetraploids due to increase of mutational target size. Moreover, mutation load increases due to relaxed purifying selection when deleterious mutations are masked by additional chromosome copies. Empirical data confirm these patterns, showing significant increase in nucleotide diversity, ratios of non-synonymous to synonymous SNPs, and number of indels and large structural variants in A. arenosa autotetraploids. However, a rather modest increase in load proxies together with a broad distribution and niche of autotetraploids suggests load accumulation has not (yet) limited their successful expansion. Overall, we demonstrate a complex interplay between neutral processes and purifying selection in shaping genetic variation following WGD and highlight ploidy as an important determinant of genetic diversity and mutation load in natural populations.