Association analyses reveal both anthropic and environmental selective events during eggplant domestication

Eggplant (Solanum melongena) is one of the four most important Solanaceous crops, widely cultivated and consumed in Asia, the Mediterranean basin, and Southeast Europe. We studied the Genome-wide association (GWA) of historical genebank phenotypic data on a genotyped worldwide collection of 3,449 eggplant accessions. A total of 334 significant associations for key agronomic traits were detected using three genome-wide association methods. Significant correlations were obtained between different types of phenotypic data, some of which were not obvious, such as between fruit size/yield and fruit color components, suggesting simultaneous anthropic selection for genetically unrelated traits. Anthropic selection of traits like leaf prickles, fruit color, and yield, acted on distinct genomic regions in the two domestication centers (South and South-East Asia), further confirming the multiple domestication of eggplant. To discriminate anthropic from environmental selection in domestication centers, we conducted a Genotype-Environment Association (GEA) on a subset of georeferenced accessions from the Indian subcontinent. The population structure in this area revealed four genetic clusters, corresponding to a latitudinal gradient, and environmental factors explained 31% of the population structure when the effect of spatial distances was removed. GEA and outlier association (OA) identified 305 candidate regions under environmental selection, containing genes for abiotic stress responses, plant development, and flowering transition. Finally, in the Indian domestication center anthropic and environmental selection acted largely independently, and on different genomic regions. These data allow a better understanding of the different effects of environmental and anthropic selection during domestication of a crop, and the different world regions where some traits were initially selected by humans.