The dynamics of introgression and parallel adaptation across North American Vitis species

Hybridization between species can contribute to parallel adaptive events. However, the prevalence of introgression is rarely measured across multiple species, meaning that it is rarely integrated with landscape-scale processes or connected to adaptive repeatability. Here we analyzed whole-genome resequencing data from 639 accessions representing 48 Vitis species. Vitis is notable for the domesticated grapevine (Vitis vinifera), multiple economically important North American species, and as an example of a temperate adaptive radiation. We reconstructed individual- and species-level phylogenetic frameworks for the genus and performed population genetic analyses for 19 species. The analyses uncovered widespread evidence of introgression, comprising ~14% of the average Vitis genome. Introgression was associated with the geographic distribution between species, and highly admixed individuals were more frequently found near ecological niche margins. Genetic analyses further indicated that previously recognized hybrid taxa, Vitis x doaniana and Vitis x champinii, likely represent ongoing hybrid swarms rather than distinct lineages. We assessed patterns of adaptive repeatability across eight species with denser population sampling. For six of eight species, most detected selective sweeps overlapped with sweeps in other species; on average, more recently diverged species shared more overlapping sweeps. A coalescence-based composite likelihood approach inferred that parallel sweep events were driven mostly by introgression, although a substantial fraction (~40%) was attributed to selection on ancestral standing variation. By integrating population genomic data across many species, this study highlights the central role of shared genetic variation-and the driving force of hybridization-across an adaptive radiation.