An ancient origin of the naked grains of maize

Abstract

Adaptation to novel environments requires genetic variation, which may either predate the novel environment or arise as new mutations. The relative importance of standing genetic variation vs. de novo mutations in adaptation remains a fundamental question in evolutionary biology. Selection during domestication has been long used as a model to understand evolutionary processes, providing information not only on the phenotypes selected but also, in many cases, an understanding of the causal loci. Of the multiple causal loci that have been identified in maize, the selected allele can be found segregating in natural populations, consistent with their origin as standing genetic variation. The sole exception to this pattern is the well-characterized domestication locus tga1, which has long been thought to be an example of selection on a de novo mutation. Here, we use a large dataset of maize and teosinte genomes to reconstruct the origin and evolutionary history of tga1. We first estimated the age of tga1-maize using a genealogy-based method, finding that the allele arose approximately 41,000-49,000 years ago, predating the beginning of maize domestication. We also identify, for the first time, tga1-maize in teosinte populations, indicating the allele can survive in the wild. Finally, we compare observed patterns of haplotype structure and mutational age distributions near tga1 with simulations, finding that patterns near tga1 in maize better resemble those generated under simulated selective sweeps on standing variation. These multiple lines of evidence suggest that maize domestication likely drew upon standing genetic variation at tga1 and cement the importance of standing variation in driving adaptation during domestication.