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Title: The interplay of demography and selection during maize domestication and expansion

Author
item WANG, LI - Iowa State University
item Beissinger, Timothy
item LORANT, ANNE - University Of California
item ROSS-IBARRA, CLAUDIA - University Of California
item ROSS-IBARRA, JEFFREY - University Of California
item HUFFORD, MATTHEW - Iowa State University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2017
Publication Date: 11/13/2017
Publication URL: https://handle.nal.usda.gov/10113/5860232
Citation: Wang, L., Beissinger, T.M., Lorant, A., Ross-Ibarra, C., Ross-Ibarra, J., Hufford, M.B. 2017. The interplay of demography and selection during maize domestication and expansion. Genome Biology. 18:215. https://doi.org/10.1186/s13059-017-1346-4.

Interpretive Summary: This study illustrates how demographic factors such as population size and how genes are distributed amongst individuals in a population over time, in combination with natural selection, have shaped diversity in maize genomes (genetic make-up) and populations in a historical context. Despite increases in the amount of maize grown since it was first domesticated, maize experienced several millennia of decline in genetic diversity after domestication and during its spread across the Americas. This “cost of domestication” has increased the prevalence of deleterious alleles (“bad” copies of genes) in maize compared to its wild ancestor (teosinte). This is particularly true in the Andes where maize appears to have undergone a dramatic loss of genetic diversity immediately after domestication in the region. During migration from its original area of domestication, certain populations of maize captured new copies (alleles) of genes from crossing with wild relatives, a process that appears to have reduced the burden of deleterious alleles. The results of this study will inform breeding decisions and protocols to improve maize production nationally and internationally.

Technical Abstract: The history of maize has been characterized by major demographic events including changes in population size associated with domestication and subsequent range expansion as well as gene flow with wild relatives. This complex demographic history and its interplay with selection have shaped diversity across maize populations and genomes. Here, we investigate these processes based on high-depth resequencing of 31 maize landraces sampled from across the pre-Columbian distribution of maize in the Americas and four wild progenitors (Zea mays ssp. parviglumis) from the Balsas River Valley in Mexico. Genome-wide demographic analyses reveal that maize domestication and geographic spread resulted in a protracted bottleneck and serial founder effects in maize, while its wild ancestor parviglumis may have experienced population growth. Compared to parviglumis, maize exhibits a genome-wide excess of deleterious alleles. Reduced diversity, higher levels of homozygosity, and an increased burden of deleterious alleles all point to a particularly extreme bottleneck associated with colonization of the Andes. Introgression is detected from the wild teosinte Zea mays ssp. mexicana into both Mexican and Guatemalan highland landraces and, to a lesser extent, maize from the highlands of the southwestern US. Introgression is found to decrease the prevalence of deleterious alleles, likely due to the higher long-term effective population size of wild maize.