The Genomic Signature of Crop-Wild Introgression in Maize

Abstract

The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize- mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Author Summary

Hybridization and introgression have been shown to play a critical role in the evolution of species. These processes can generate the diversity necessary for novel adaptations and continued diversification of taxa. Previous research has suggested that not all regions of a genome are equally permeable to introgression. We have conducted one of the first genome-wide assessments of patterns of reciprocal introgression in plant populations. We found evidence that suggests domesticated maize received adaptation to highland conditions from a wild relative, teosinte, during its spread to the high elevations of central Mexico. Gene flow appeared asymmetric, favoring teosinte introgression into maize, and was widespread across populations at putatively adaptive loci. In contrast, genomic regions near known domestication and cross-incompatibility loci appeared particularly resistant to introgression in both directions of gene flow. Crop-wild study systems should play an important role in future studies of introgression due to their well-developed genomic resources and histories of reciprocal gene flow during crop expansion.