The interplay of demography and selection during maize domestication and expansion

The history of maize has been characterized by major demographic events including changes in population size associated with domestication and range expansion as well as gene flow with wild relatives. The interplay between demographic history and selection has shaped diversity across maize populations and genomes. Here, we investigate these processes based on high-depth resequencing data from 31 maize landraces spanning the pre-Columbian distribution of maize as well as four wild progenitor individuals (Zea mays ssp. parviglumis) from the Balsas River Valley in Mexico. Genome-wide demographic analyses reveal that maize domestication and spread resulted in pronounced declines in effective population size due to both a protracted bottleneck and serial founder effects, while, concurrently, parviglumis experienced population growth. The cost of maize domestication and spread was an increase in deleterious alleles in the domesticate relative to its wild progenitor. This cost is particularly pronounced in Andean maize, which appears to have experienced a more dramatic founder event when compared to other maize populations. Introgression from the wild teosinte Zea mays ssp. mexicana into maize in the highlands of Mexico and Guatemala is found found to decrease the prevalence of deleterious alleles, likely due to the higher long-term effective population size of wild maize. These findings underscore the strong interaction between historical demography and the efficiency of selection species- and genome-wide and suggest domesticated species with well-characterized histories may be particularly useful for understanding this interplay.