Selective sorting of ancestral introgression in maize and teosinte along an elevational cline

Abstract

While often deleterious, hybridization can also be a key source of genetic variation and pre-adapted haplotypes, enabling rapid evolution and niche expansion. Here we evaluate these opposing selection forces on introgressed ancestry between maize (Zea mays ssp. mays) and its wild teosinte relative, mexicana (Zea mays ssp. mexicana). Introgression from ecologically diverse teosinte may have facilitated maizes global range expansion, in particular to challenging high elevation regions (> 1500 m). We generated low-coverage genome sequencing data for 348 maize and mexicana individuals to evaluate patterns of introgression in 14 sympatric population pairs, spanning the elevational range of mexicana, a teosinte endemic to the mountains of Mexico. While recent hybrids are commonly observed in sympatric populations and mexicana demonstrates fine-scale local adaptation, we find that the majority of mexicana ancestry tracts introgressed into maize over 1000 generations ago. This mexicana ancestry seems to have maintained much of its diversity and likely came from a common ancestral source, rather than contemporary sympatric populations, resulting in relatively low FSTbetween mexicana ancestry tracts sampled from geographically distant maize populations. Introgressed mexicana ancestry in maize is reduced in lower-recombination rate quintiles of the genome and around domestication genes, consistent with pervasive selection against introgression. However, we also find mexicana ancestry increases across the sampled elevational gradient and that high introgression peaks are most commonly shared among high-elevation maize populations, consistent with introgression from mexicana facilitating adaptation to the highland environment. In the other direction, we find patterns consistent with adaptive and clinal introgression of maize ancestry into sympatric mexicana at many loci across the genome, suggesting that maize also contributes to adaptation in mexicana, especially at the lower end of its elevational range. In sympatric maize, in addition to high introgression regions we find many genomic regions where selection for local adaptation maintains steep gradients in introgressed mexicana ancestry across elevation, including at least two inversions: the well-characterized 14 Mb Inv4m on chromosome 4 and a novel 3 Mb inversion Inv9f surrounding the macrohairless1 locus on chromosome 9. Most outlier loci with high mexicana introgression show no signals of sweeps or local sourcing from sympatric populations and so likely represent ancestral introgression sorted by selection, resulting in correlated but distinct outcomes of introgression in different contemporary maize populations. Author SummaryWhen species expand their ranges, new encounters with diverse wild relatives can introduce deleterious genetic variation, but may also accelerate the colonization of novel environments by providing ready-made genetic adaptations. Maize today is a global staple, far exceeding the original ecological niche of its wild progenitor. We show that gene flow from highland-endemic wild mexicana facilitated maizes range expansion from the valleys where it was domesticated to sites over 1500m in the mountains of Mexico. We find loci where mexicana ancestry has been repeatedly favored in highland maize populations. We also find loci (including a newly identified inversion) where mexicana ancestry increases steeply with elevation, providing evidence for adaptive trade-offs. We additionally demonstrate selection against mexicana ancestry, especially near domestication genes. We sampled mexicana growing alongside maize fields, yet find little evidence that introgression is recent or locally-sourced genomewide or at adaptive loci. Rather, the majority of mexicana ancestry was introduced into maize over 1000 generations ago, and subsequently diverged and was sorted by selection in individual populations. These results add to our understanding of the effects of introgression on range expansions and adaptation.