The interplay of demography and selection during maize domestication and expansion.

BACKGROUND: The history of maize has been characterized by major demographic events, including population size changes associated with domestication and range expansion, and gene flow with wild relatives. The interplay between demographic history and selection has shaped diversity across maize populations and genomes. RESULTS: We investigate these processes using high-depth resequencing data from 31 maize landraces spanning the pre-Columbian distribution of maize, and four wild teosinte individuals (Zea mays ssp. parviglumis). Genome-wide demographic analyses reveal that maize experienced pronounced declines in effective population size due to both a protracted domestication bottleneck and serial founder effects during post-domestication spread, while parviglumis in the Balsas River Valley experienced population growth. The domestication bottleneck and subsequent spread led to an increase in deleterious alleles in the domesticate compared to the wild progenitor. This cost is particularly pronounced in Andean maize, which has experienced a more dramatic founder event compared to other maize populations. Additionally, we detect introgression from the wild teosinte Zea mays ssp. mexicana into maize in the highlands of Mexico, Guatemala, and the southwestern USA, which reduces the prevalence of deleterious alleles likely due to the higher long-term effective population size of teosinte. CONCLUSIONS: These findings underscore the strong interaction between historical demography and the efficiency of selection and illustrate how domesticated species are particularly useful for understanding these processes. The landscape of deleterious alleles and therefore evolutionary potential is clearly influenced by recent demography, a factor that could bear importantly on many species that have experienced recent demographic shifts.

Megabase-scale inversion polymorphism in the wild ancestor of maize.

Chromosomal inversions are thought to play a special role in local adaptation, through dramatic suppression of recombination, which favors the maintenance of locally adapted alleles. However, relatively few inversions have been characterized in population genomic data. On the basis of single-nucleotide polymorphism (SNP) genotyping across a large panel of Zea mays, we have identified an ∼50-Mb region on the short arm of chromosome 1 where patterns of polymorphism are highly consistent with a polymorphic paracentric inversion that captures >700 genes. Comparison to other taxa in Zea and Tripsacum suggests that the derived, inverted state is present only in the wild Z. mays subspecies parviglumis and mexicana and is completely absent in domesticated maize. Patterns of polymorphism suggest that the inversion is ancient and geographically widespread in parviglumis. Cytological screens find little evidence for inversion loops, suggesting that inversion heterozygotes may suffer few crossover-induced fitness consequences. The inversion polymorphism shows evidence of adaptive evolution, including a strong altitudinal cline, a statistical association with environmental variables and phenotypic traits, and a skewed haplotype frequency spectrum for inverted alleles.