Meiotic Adaptation to Whole-Genome Duplication in Arabidopsis arenosa

Whole genome duplication (WGD) is a major factor in evolution, adaptation and speciation. Yet by doubling the number of homologs present, WGD challenges reliable chromosome segregation, a process conserved across eukaryotes. Through its negative effects on chromosome segregation, WGD can contribute to aneuploidy and infertility, and in humans, cancer progression and spontaneous abortion. Nevertheless, numerous genome-duplicated (polyploid) species persist in nature, particularly among plants, and most have stable, often diploid like chromosome segregation, indicating that early problems can be overcome. Currently very little is known about which genes or processes may be under selection after WGD to stabilize chromosome segregation—only one has been molecularly characterized to date. We use Arabidopsis arenosa, an outcrossing relative of A. thaliana with extant diploid and polyploid populations, to better understand the genic basis of adaptation to polyploidy. First, we show that newly doubled diploid A. arenosa has extensive multivalent formation in diakinesis and metaphase I, while the natural autotetraploid has stable bivalent formation. This is coupled with a reduction in crossover formation in the natural tetraploid relative to the diploid. Second, in a genome scan we show that although most polymorphism is shared across ploidies, there is strong ploidy-associated allelic differentiation in 44 genes with discrete, mostly single-gene peaks of sharply elevated differentiation. Among these are eight meiosis genes encoding proteins that coordinate a specific subset of early meiotic functions that affect chromosome pairing, synapsis, and the number and distribution of chiasmata. Third, we show evidence for one gene that the derived allele has a functional consequence in tetraploid meiosis. We hypothesize that these genes represent a polygenic solution to WGD-associated chromosome segregation challenges.