Repeated domestication shaped the evolution of grain amaranth in Mesoamerica

Grain amaranths are nutritious pseudocereals that have been domesticated in the Andes and Mesoamerica. The three grain amaranth species were probably domesticated independently from Amaranthus hybridus in different geographical regions. Although the domestication process across the three grain amaranths has been partially elucidated, the history within each domesticated species remains vastly unknown. Therefore, we study the origin and domestication history of A. cruentus within Mesoamerica. We reveal a high genetic diversity and distinct histories of subgroups, using whole genome sequencing of 138 accessions belonging to A. cruentus and its closely related species (A. hypochondriacus) along with the wild relative A. hybridus mainly from the South of Mexico and Guatemala. We identified three genetic groups of A. cruentus. Amaranthus cruentus group 1, representing the center of Mexico, A. cruentus group 2 mostly from Guatemala, and A. cruentus group 3, including individuals dispersed across Mexico, but distinct from group 1. Compared to A. hybridus, A. cruentus group 3 exhibited the lowest genetic differentiation. It had the highest genetic diversity among the A. cruentus groups. We find gene flow between A. cruentus group 1 and A. hybridus indicating the ongoing interbreeding between wild and domesticated amaranth in its domestication center. Our results suggest that A. cruentus was probably first domesticated in central Mexico and secondary population in Guatemala, where this species is most widely preferred and cultivated today. Our findings help elucidate the complex history of grain amaranth in the Americas and underline the non-linear nature of domestication.