The History of Lentil (Lens culinaris subsp. culinaris) Domestication and Spread as Revealed by Genotyping-by-Sequencing of Wild and Landrace Accessions

Abstract

Protein-rich legumes accompanied carbohydrate-rich cereals since the beginning of agriculture and yet their domestication history is not as well understood. Lentil (Lens culinaris Medik. subsp. culinaris) was first cultivated in Southwest Asia (SWA) 8000–10,000 years ago but archeological evidence is unclear as to how many times it may have been independently domesticated, in which SWA region(s) this may have happened, and whether wild species within the Lens genus have contributed to the cultivated gene pool. In this study, we combined genotyping-by-sequencing (GBS) of 190 accessions from wild (67) and domesticated (123) lentils from the Old World with archeological information to explore the evolutionary history, domestication, and diffusion of lentils to different environments. GBS led to the discovery of 87,647 single-nucleotide polymorphisms (SNPs), which allowed us to infer the phylogeny of genus Lens. We confirmed previous studies proposing four groups within it. The only gene flow detected was between cultivated varieties and their progenitor (L. culinaris subsp. orientalis) albeit at very low levels. Nevertheless, a few putative hybrids or naturalized cultivars were identified. Within cultivated lentil, we found three geographic groups. Phylogenetics, population structure, and archeological data coincide in a scenario of protracted domestication of lentils, with two domesticated gene pools emerging in SWA. Admixed varieties are found throughout their range, suggesting a relaxed selection process. A small number of alleles involved in domestication and adaptation to climatic variables were identified. Both novel mutation and selection on standing variation are presumed to have played a role in adaptation of lentils to different environments. The results presented have implications for understanding the process of plant domestication (past), the distribution of genetic diversity in germplasm collections (present), and targeting genes in breeding programs (future).