The Evolutionary Genomics of Grape (Vitis viniferassp.vinifera) Domestication

ABSTRACT We gathered genomic data from grapes ( Vitis vinifera ssp. vinifera ), a clonally propagated perennial crop, to address three ongoing mysteries about plant domestication. The first is the duration of domestication; archaeological evidence suggests that domestication occurs over millennia, but genetic evidence indicates it can occur rapidly. We estimated that our wild and cultivated grape samples diverged ~22,000 years ago and that the cultivated lineage experienced a steady decline in population size ( N e ) thereafter. The long decline may reflect low intensity management by humans prior to domestication. The second mystery is the identification of genes that contribute to domestication phenotypes. In cultivated grapes, we identified candidate-selected genes that function in sugar metabolism, flower development and stress responses. In contrast, candidate selected genes in the wild sample were limited to abiotic and biotic stress responses. A genomic region of high divergence corresponded to the sex determination region and included a candidate male sterility factor and additional genes with sex-specific expression. The third mystery concerns the cost of domestication. Annual crops accumulate putatively deleterious variants, in part due to strong domestication bottlenecks. The domestication of perennial crops differs from annuals in several ways, including the intensity of bottlenecks, and it is not yet clear if they accumulate deleterious variants. We found that grape accessions contained 5.2% more deleterious variants than wild individuals, and these were more often in a heterozygous state. Using forward simulations, we confirm that clonal propagation leads to the accumulation of recessive deleterious mutations but without decreasing fitness. Significance Statement We generated genomic data to estimate the population history of grapes, the most economically important horticultural crop in the world. Domesticated grapes experienced a protracted, 22,000 year population decline prior to domestication; we hypothesize that this decline reflects low intensity cultivation by humans prior to domestication. Domestication altered the mating system of grapes. The sex determination region is detectable as a region of heightened genetic divergence between wild and cultivated accessions. Based on gene expression analyses, we propose new candidate genes that alter sex determination. Finally, grapes contain more deleterious mutations in heterozygous states than their wild ancestors. The accumulation of deleterious mutations is due in part to clonal propagation, which shelters deleterious, recessive mutations.