Parallel Seed Color Adaptation during Multiple Domestication Attempts of an Ancient New World Grain

Thousands of plants have been selected as crops; yet, only a few are fully domesticated. The lack of adaptation to agroecological environments of many crop plants with few characteristic domestication traits potentially has genetic causes. Here, we investigate the incomplete domestication of an ancient grain from the Americas, amaranth. Although three grain amaranth species have been cultivated as crop for millennia, all three lack key domestication traits. We sequenced 121 crop and wild individuals to investigate the genomic signature of repeated incomplete adaptation. Our analysis shows that grain amaranth has been domesticated three times from a single wild ancestor. One trait that has been selected during domestication in all three grain species is the seed color, which changed from dark seeds to white seeds. We were able to map the genetic control of the seed color adaptation to two genomic regions on chromosomes 3 and 9, employing three independent mapping populations. Within the locus on chromosome 9, we identify an MYB-like transcription factor gene, a known regulator for seed color variation in other plant species. We identify a soft selective sweep in this genomic region in one of the crop species but not in the other two species. The demographic analysis of wild and domesticated amaranths revealed a population bottleneck predating the domestication of grain amaranth. Our results indicate that a reduced level of ancestral genetic variation did not prevent the selection of traits with a simple genetic architecture but may have limited the adaptation of complex domestication traits.