Evolutionary genomics of grape (Vitis vinifera ssp. 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 that 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 before 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 that of 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.

Keywords: candidate genes; clonal propagation; deleterious variants; demography; sex determination.

Fig. 1.

Population structure of cultivated and wild samples. (A) PCA plot based on genetic covariance among all individuals of wild samples (red) and cultivars (green for wine grapes and blue for table grapes). (B) Neighbor-joining tree across all samples, rooted by V. rotundifolia.

Fig. 2.

Intra- and intertaxon analyses of demographic history and divergence. (A) MSMC estimates of the effective population size (N_e) of vinifera based on two separate runs of four individuals. The solid line represents wine grapes, and the dashed line is table grapes. (B) MSMC analysis of cross-coalescence (y axis) based on comparisons between sylvestris and either wine or table grapes. (C) Divergence time and past N_e changes inferred by the SMC++ analyses, based on unphased genotypes.

Fig. 3.

The CLR statistic computed for 20-kbp windows along chromosomes separately for wild samples and cultivars. (A) The scatterplot shows the CLR statistic for corresponding windows for both wild (x axis) and cultivated samples (y axis). The dashed line represents the 99.5% cutoff, and red dots represent outlier regions. (B) F_ST analyses between vinifera and sylvestris identify two peaks in the sex determination region that encompass 45 annotated genes.

Fig. 4.

The number and frequency of derived deleterious alleles in cultivars and wild samples. (Top) Comparisons between vinifera and sylvestris for the number of deleterious variants per individual overall (Left), as homozygotes (Middle), and as heterozygotes (Right). (Bottom) Comparisons between sweep regions and the rest of the genome (control) for the number (Left), population frequency (Middle), and ratio (Right) of the number deleterious to synonymous variants per vinifera individual.

Fig. 5.

Forward simulations under a model of recessive selection for three demographic scenarios and two mating systems. (Top) The average number of deleterious alleles per accession relative to an outcrossing population of constant size. (Bottom) The total load relative to an outcrossing population of constant size. The dashed lines represent the time of demographic shift, ∼30 kya, and the onset of clonal propagation during domestication ∼8 kya. Bot, bottleneck; Clo, clonal propagation; Con, constant population size; Dec, declining population size; Out, outcrossing.