Selective sorting of ancestral introgression in maize and teosinte along an elevational cline
Authors: Calfee Erin , Gates Daniel , Lorant Anne , Perkins M. Taylor , Coop Graham , Ross-Ibarra Jeffrey 
Published: March 2021

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 maysssp.mays) and its wild teosinte relative,mexicana(Zea maysssp.mexicana). Introgression from ecologically diverse teosinte may have facilitated maize’s global range expansion, in particular to challenging high elevation regions (>1500 m). We generated low-coverage genome sequencing data for 348 maize andmexicanaindividuals to evaluate patterns of introgression in 14 sympatric population pairs, spanning the elevational range ofmexicana, a teosinte endemic to the mountains of Mexico. While recent hybrids are commonly observed in sympatric populations andmexicanademonstrates fine-scale local adaptation, we find that the majority ofmexicanaancestry tracts introgressed into maize over 1000 generations ago. Thismexicanaancestry seems to have maintained much of its diversity and likely came from a common ancestral source, rather than contemporary sympatric populations, resulting in relatively lowFSTbetweenmexicanaancestry tracts sampled from geographically distant maize populations.

Introgressedmexicanaancestry 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 findmexicanaancestry increases across the sampled elevational gradient and that high introgression peaks are most commonly shared among high-elevation maize populations, consistent with introgression frommexicanafacilitating adaptation to the highland environment. In the other direction, we find patterns consistent with adaptive and clinal introgression of maize ancestry into sympatricmexicanaat many loci across the genome, suggesting that maize also contributes to adaptation inmexicana, 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 introgressedmexicanaancestry across elevation, including at least two inversions: the well-characterized 14 MbInv4mon chromosome 4 and a novel 3 Mb inversionInv9fsurrounding themacrohairless1locus on chromosome 9. Most outlier loci with highmexicanaintrogression 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 Summary

When 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 wildmexicanafacilitated maize’s range expansion from the valleys where it was domesticated to sites over 1500m in the mountains of Mexico. We find loci wheremexicanaancestry has been repeatedly favored in highland maize populations. We also find loci (including a newly identified inversion) wheremexicanaancestry increases steeply with elevation, providing evidence for adaptive trade-offs.

We additionally demonstrate selection againstmexicanaancestry, especially near domestication genes. We sampledmexicanagrowing alongside maize fields, yet find little evidence that introgression is recent or locally-sourced genomewide or at adaptive loci. Rather, the majority ofmexicanaancestry 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.