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. 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 Zea mays ssp. 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 >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 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 Inv4m and a new 3 Mb inversion Inv9f surrounding the macrohairless1 locus on chromosome 9. The bulk of our ancestry selection outliers 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 landrace populations.

The genomic consequences of hybridization

“…Even after genome-wide admixture proportions have stabilized, theory predicts that minor-parent ancestry will be more fully removed from regions of the genome with low recombination rates ( Wu, 2001 ; Nachman and Payseur, 2012 ). Data from diverse taxa, including swordtail fishes, humans, monkeyflowers, maize, and Heliconius butterflies ( Schumer et al, 2018 ; Calfee, 2021 ; Edelman et al, 2019 ; Brandvain et al, 2014 ; Martin et al, 2019 ), support this theoretical prediction (but see Corbett-Detig and Nielsen, 2017 ). However, differing correlations between recombination rate and gene density can lead to local differences in minor parent ancestry, depending on where in the genome recombination primarily occurs.…”

“…Although the sources of selection on hybrids undoubtedly differ between species ( Juric et al, 2016 ; Schumer et al, 2018 ; Brandvain et al, 2014 ), studies across diverse taxa have largely found that regions of the genome that are dense in coding or conserved elements tend to be particularly resistant to movement between species ( Sankararaman et al, 2014 ; Teeter et al, 2008 ; Turissini and Matute, 2017 ; Martin et al, 2013 ; Calfee, 2021 ; Brandvain et al, 2014 ; Masly and Presgraves, 2007 ; Maxwell et al, 2018 ). In the case of conserved regulatory elements in humans, this pattern is stronger at enhancers that harbor derived mutations as opposed to ancestral variants ( Telis et al, 2020 ).…”

“…Given broad selection against minor parent ancestry, adaptive introgression is often occurring against a background of genome-wide purging ( Calfee, 2021 ; Edelman et al, 2019 ; Turner and Harr, 2014 ). In some cases, this has made adaptively introgressed haplotypes easy to identify empirically since they form peaks of high minor parent ancestry against a background of low minor parent ancestry ( Sankararaman et al, 2014 ; Vernot and Akey, 2014 ).…”

“…Some of this genetic exchange reflects the process of adaptive introgression , which has been well-documented in several species ( Marques et al, 2019 ; Hedrick, 2013 ; Racimo et al, 2015 ). However, the introgression of adaptive and neutral variants occurs against the backdrop of broad, genome-wide selection against hybrids ( Orr, 1995 ; Arnegard et al, 2014 ; Svedin et al, 2008 ; Christie and Strauss, 2018 ) and hybridization-derived regions in the genome ( Sankararaman et al, 2014 ; Juric et al, 2016 ; Harris and Nielsen, 2016 ; Schumer et al, 2018 ; Calfee, 2021 ). The mechanisms resulting in lower fitness of hybrids are diverse, ranging from ecological selection against hybrids, to differences in the number of deleterious variants harbored by the hybridizing species (known as hybridization load ), to negative interactions between genes derived from the two parental species’ genomes ( hybrid incompatibilities ).…”

“…Because many factors interact simultaneously in hybrids, genome evolution is unusually dynamic after hybridization. In the last several years, the community has shifted from describing the presence of admixture in the genomes of diverse species to documenting patterns of local variation in ancestry along the genome ( Sankararaman et al, 2014 ; Sankararaman et al, 2016 ; Schumer et al, 2018 ; Calfee, 2021 ; Edelman et al, 2019 ; Brandvain et al, 2014 ; Kulmuni et al, 2020 ; Runemark et al, 2018 ). One common observation from these cases is that, on average, selection acts to remove ancestry from the minor parent (i.e., the species from which hybrids derive less of their genome) in the most functionally important regions of the genome.…”