A Tomato Genome From The Italian Renaissance Provides Insights Into Columbian and Pre-Columbian Exchange Links And Domestication

A bstract The history of the tomato’s interactions with humans spans both a pre-Columbian period of millennia of cultivation and domestication in South and Central America as well as the plant’s rise to becoming one of the world’s major cash crops following the arrival of Europeans in the Neotropics and the subsequent Columbian Exchange. In the process, the influence of successive regimes of artificial selection gave rise to an entangled species complex comprised of a wild ancestor and numerous cultivars exhibiting a great diversity of fruit phenotypes (often sorted in ‘cherry’ and big types). Here, we provide a snapshot into these dynamics by presenting the ancient nuclear and plastid genomes of one of the oldest tomatoes still in existence: the almost half a millennium old En Tibi specimen from the Italian Renaissance. By placing the genome skimming data obtained from this specimen within the phylogenomic context of wild relatives and Neotropical tomato cultivars and land races, we are able to show that the most likely geographic origins of the specimen’s immediate ancestors, i.e. whence the exchange of this particular lineage originated, are around the Gulf of Mexico. We also show that this specimen was less inbred than present-day tomatoes, shedding light on the genomic signatures of historical domestication processes. Probing deeper into the ancestry that shaped extant genetic diversity within the complex, we reconstruct multiple ancestral populations with diffuse but distinct signatures in cherry and big tomatoes. The geographic structure of these ancestries within the nearest wild relative of tomatoes and the differential extent to which these ancestries are represented in domesticates points to early cultivation and human-assisted dispersal of tomatoes originating from the northern extreme of the natural range of the species. Our findings illustrate the inferences that can be drawn from ancient DNA extracted from herbarium specimens and historic plant collections. At the same time, we stress that our findings draw on multiple disciplines including ethnobotanical and historical research and on the (agri)cultural contributions of a variety of world cultures.