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 maize’s 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 FST between 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.

Predictability and parallelism in the contemporary evolution of hybrid genomes

“…We next evaluated correlations between minor parent ancestry and genomic features known to interact with selection in other hybrid systems. Studies in a number of systems have found that selection on hybrids can drive a positive correlation between recombination rate and minor parent ancestry [8,35,36,40]. Using averages of minor parent ancestry and recombination rate summarized in non-overlapping windows we found strong evidence that recombination rate is positively correlated with minor parent ancestry at both a local (Fig.…”

“…Notably, three shared minor parent islands occur in inversions that differentiate species, conflicting with the prevailing wisdom that inversions should resist introgression (Fig. S18; see [40,56,57] for similar findings).…”

“…2). This represents at least the sixth system in which these effects have been detected [8,12,35,36,38,40], suggesting that these patterns of selection on minor parent ancestry are predictable outcomes of the process of genome stabilization after hybridization.…”

“…Intriguingly, inversions that differed between species had unusually high minor parent ancestry in all hybrid populations on average (Fig. S19), in contrast to what is most frequently observed in other systems ( [53][54][55] but see [40,56,57]).…”

“…These include broad selection against minor parent ancestry across the genome (presumably due to the mechanisms outlined above) and stronger depletion of minor parent ancestry in regions of the genome with a high density of conserved or coding elements [8,12,35,36]. Another key variable highlighted by empirical and theoretical studies is the importance of the interplay between recombination rate and selection, with several groups finding that selection on hybrids generates a positive correlation between local recombination rate and minor parent ancestry [8,[35][36][37][38][39][40][41]. This correlation is thought to be driven by how the local recombination rate impacts the decoupling of neutral or adaptive alleles from alleles that are deleterious in hybrids.…”