Genetic incompatibilities and evolutionary rescue by wild relatives shaped grain amaranth domestication

Abstract

Crop domestication and the subsequent expansion of crops have long been thought of as a linear process from a wild ancestor to a domesticate. However, evidence of gene flow from locally adapted wild relatives that provided adaptive alleles into crops has been identified in multiple species. Yet, little is known about the evolutionary consequences of gene flow during domestication and the interaction of gene flow and genetic load in crop populations. We study the pseudo-cereal grain amaranth that has been domesticated three times in different geographic regions of the Americas. We quantify the amount and distribution of gene flow along the genome of the three grain amaranth species and their two wild relatives. Our results show ample gene low between crop species and between crops and their wild relatives. Genetic load in introgressed regions from different donors suggest the potential of evolutionary rescue through decreased genetic load in genomic regions contributed by wild relatives with larger population size. To assess fitness of early hybrids we performed experimental crosses between the three crop species and found genetic incompatibilities between one Central American grain amaranth and the other two crop species. These incompatibilities might have created recent reproductive barriers, and maintain species integrity today. Together, our results show that gene flow played an important role in the domestication and expansion of grain amaranth, despite genetic species barriers. The domestication of plants was likely not linear and created a genomic mosaic by multiple contributors with varying fitness effects for today's crops.