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

['Erin Calfee', 'Center For Population Biology', 'University Of California', 'Davis', 'California', 'United States Of America', 'Department Of Evolution', 'Ecology', 'Daniel Gates', 'Anne Lorant']

Date: 2021-12

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.

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 F ST between mexicana ancestry tracts sampled from geographically distant maize populations.

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.

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 wild mexicana facilitated maize’s 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.

Funding: This work was funded by the the Division of Integrative Organismal Systems from the National Science Foundation, www.nsf.gov (NSF No. 1546719, awarded to JRI and GC), the National Institute of General Medical Sciences of the National Institutes of Health, www.nigms.nih.gov (NIH R01 GM108779 and R35 GM136290, awarded to GC), and the University of California, Davis, https://ucdavis.edu (Loomis Graduate Fellowship in Agronomy, awarded to EC). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability: Raw Illumina sequence data generated by this study is available through the NCBI Short Read Archive, PRJNA657016 (maize/mexicana) and SRR7758238 (Tripsacum). All relevant metadata is found within the Supporting information files. Access to previously published genomic resources used in this study: B73 maize reference genome v4 (Gramene), recombination map from Ogut et al. 2015 ( https://www.panzea.org/publications ), maize reference panel sequences (NCBI SRA PRJNA616247), and parviglumis reference panel sequences (NCBI SRA PRJNA616247). Local ancestry posterior probability files, ancestry_hmm input files, genomewide ancestry estimates, and summarised population allele frequency data are accessible via Figshare ( https://doi.org/10.6084/m9.figshare.16641799 ). Scripts are available at https://github.com/ecalfee/hilo .

Copyright: © 2021 Calfee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

In this study, we generate whole genome sequencing data to investigate genomic signatures of admixture and selection in paired sympatric maize and mexicana populations, sampled from 14 locations across an elevational gradient in Mexico. Mexicana was sampled from wild populations and maize was sampled from nearby fields where traditional cultivation methods and open pollination have resulted in populations with distinct local characteristics and high phenotypic and genetic diversity (often called maize ‘landraces’). This expanded sampling of sympatric maize and mexicana populations across Mexico, combined with genomewide data and a well-parameterized null model, improves our ability to more formally test for adaptive introgression and identify likely source populations. The source of introgression is of interest, as teosinte demonstrates local adaptation to different niches within the highlands and there is significant genetic structure between mexicana ecotypes [ 32 , 37 , 49 – 51 ]. Thus we can test whether local mexicana populations are the ongoing source for geographically-restricted locally adaptive haplotypes. We use this comprehensive genomic dataset to characterize the bi-directional timing and origin of introgression and evaluate the patterns and scale of natural selection for and against admixture between these taxa.

While some highland and locally-adapted alleles may be beneficial to maize, many introgressed mexicana alleles, especially those affecting domestication traits, should be selected against by farmers growing maize. In addition, maize alleles introgressed into mexicana should be selected against because maize has accumulated genetic load from reduced population sizes during domestication [ 44 ] and because domestication traits generally reduce fitness in the wild [ 46 – 48 ], e.g. loss of disarticulation and effective seed dispersal [ 37 ].

Maize was introduced as a crop to the mountains of Mexico around 6.2 thousand years ago [ 36 ], and it is thought that gene flow from mexicana assisted in adaptation to high elevation selection pressures. Highland maize and mexicana share a number of putatively adaptive phenotypes [ 37 , 38 ], including earlier flowering times for the shorter growing season [ 34 ], purple anthocyanin-based pigmentation which shields DNA from UV damage [ 39 ] and increases solar heat absorption [ 40 ], and macrohairs on the leaf and stem sheath, which are thought to increase herbivore defense [ 41 ] and/or heat maintenance in colder environments [ 42 ]. Earlier studies using 50K SNP-chip data for highland populations [ 43 ] or genomewide data for a small number of individuals [ 44 , 45 ], have shown that highland maize populations have experienced significant admixture from mexicana, reaching high frequency at some loci, consistent with adaptive introgression.

Maize (Zea mays ssp. mays) is an ideal system to study selection on admixed ancestry and the effects on range expansion, as it has colonized nearly every human-inhabited ecosystem around the world [ 25 ] and interbreeds with a number of wild relatives genetically adapted to distinct ecologies [ 26 , 27 ]. In Mexico, highland maize represents an early major niche expansion that may have been facilitated by introgression. Approximately 9 thousand years ago, maize (Zea mays ssp. mays) was domesticated in the Balsas River Valley in Mexico from a lowland-adapted sub-species of teosinte (Zea mays ssp. parviglumis [ 28 ]), which grows readily at sea level and lower elevations of the Sierra Madre del Sur [ 29 ]. In contrast, Zea mays ssp. mexicana, which diverged from parviglumis about 60 thousand years ago [ 30 ], is endemic to highland regions in Mexico (∼1500–3000 meters in elevation) where it has adapted to a number of ecological challenges: a cooler, drier climate with higher UV intensity, different soil nutrient composition, and a shorter growing season necessitating earlier flowering times [ 31 – 35 ].

Interbreeding between partially diverged species or subspecies can result in admixed individuals with low fitness, e.g. due to hybrid incompatibilities [ 1 – 3 ]. Consistent with the view that hybridization is often deleterious, a growing number of species show evidence of pervasive selection against introgressed ancestry [ 4 – 13 ]. At the same time, introgression can be a source of novel genetic variation and efficiently introduce haplotypes carrying sets of locally adapted alleles, with the potential for rapid adaptation to new ecological challenges [ 14 ]. Indeed, admixture has been linked to adaptive species radiations and/or rapid niche expansions in a number of natural systems, including mosquitoes [ 15 ], Drosophila [ 16 ], butterflies [ 9 ], cichlids [ 17 ], sunflowers [ 18 ], wild tomatoes [ 19 ] and yeast [ 20 , 21 ]. In addition, introgression from wild relatives has facilitated the broad range expansions of multiple domesticated crops (reviewed in [ 22 ] and [ 23 ]), and gene flow from crops back into their wild relatives has in some cases opened up novel ‘weedy’ niches [ 24 ].

Results/discussion

Genomewide mexicana ancestry is structured by elevation We sampled paired sympatric populations from 14 geographically dispersed locations to assess the extent of gene flow between maize and mexicana in Mexico. Maize today is grown across the entire elevational range of its wild teosinte relatives, from sea-level up to 4000 meters [52]. Our sampled sites range from 1547–2600 meters in elevation, which spans a large portion of mexicana’s range and exceeds the upper elevational range for maize’s wild ancestor, parviglumis (Fig 1). For each of 14 maize/mexicana sympatric sample locations, we resequenced 7–15 individuals per subspecies. PPT PowerPoint slide

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TIFF original image Download: Fig 1. Sampled sympatric maize/mexicana populations compared to the distribution of teosintes. (A) Elevational range of teosintes based on historical occurrence data (1842–2016) from [29]. Parviglumis and mexicana overlap at middle elevations (dark green) and maize today is grown across this entire elevational range. (B) Geographic location and elevation of contemporary sympatric maize and mexicana population pairs sampled across 14 sites. Map of Mexico created with Natural Earth data (https://www.naturalearthdata.com). https://doi.org/10.1371/journal.pgen.1009810.g001 We additionally sequenced 43 individuals from 3 mexicana reference populations, totalling 348 low-coverage genomes (mean ∼1x). Two of these mexicana reference populations are documented to have no adjacent maize agriculture within the past 50 years, while a third higher elevation population (Amecameca) was chosen because it grows above the elevational range of parviglumis, and thus outside of the historical range of maize. For a maize reference population, we added 55 previously published high-coverage genomes from a population grown near Palmar Chico at 983 m [53, 54], well below the elevational range of mexicana. Because parviglumis is known to admix historically with both of our focal subspecies in Mexico, we also included 50 previously published high-coverage parviglumis genomes from the ‘Mound’ population at 1,008 m, also near Palmar Chico [53–55]. Completely allopatric reference populations are not available because maize has been grown at high density throughout Mexico across the full elevational range of both teosintes. A priori, gene flow from maize into mexicana is possible at Amecameca, and historically between maize and teosinte at all locations. We therefore assess for possible gene flow into each reference population below. Principal components analysis of genetic diversity clearly separates maize and mexicana, with putative admixed individuals from sympatric populations having intermediate values along PC1. Additionally, PC2 provides evidence of gene flow from parviglumis, particularly into lower elevation mexicana populations (S1 Fig), which motivated us to analyse a 3-way admixture scenario in all subsequent analyses. To estimate genomewide ancestry proportions for each individual, we ran NGSAdmix [56] with K = 3 genetic clusters and genotype likelihoods for all mexicana, maize, and parviglumis individuals. The three genetic clusters clearly map onto mexicana, maize and parviglumis ancestry, with no significant admixture in the lowland maize or parviglumis reference populations. We find minority parviglumis ancestry in the two lower-elevation reference mexicana populations, but no evidence of introgression from parviglumis or maize into the highest elevation population at Amecameca (Fig 2A). PPT PowerPoint slide

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TIFF original image Download: Fig 2. Distribution of mexicana ancestry by elevation. (A) Genomewide ancestry estimates (NGSAdmix) for reference maize, mexicana and parviglumis individuals, grouped by sampling location. (B) Genomewide mexicana ancestry estimates (NGSAdmix) for sympatric maize and mexicana individuals (n = 305) along an elevational gradient, colored by sampling location. Lines show best linear model fit for mexicana ancestry by elevation for each subspecies separately. https://doi.org/10.1371/journal.pgen.1009810.g002 Looking across samples from the 14 sympatric sites, we find a positive association between ancestry proportion and elevation (km), with higher mexicana ancestry at higher elevations in both sympatric maize (β = 0.22, P = 1.01 × 10−31) and sympatric mexicana (β = 0.32, P = 2.02 × 10−38) individuals (Fig 2B). Increasing mexicana ancestry at higher elevations is consistent with selection favoring mexicana ancestry at higher elevations, but could also be due to purely demographic processes, e.g. a higher density of (wind-dispersed) mexicana pollen at higher elevations, or increased gene flow from non-admixed maize populations at lower elevations. While most populations have admixture proportions well-predicted by their elevation, outlier populations may be the result of recent colonization histories for some locations or adaptation to other environmental niches. Within teosintes, elevation is a major axis of niche separation between parviglumis (the ancestor of maize) and mexicana [50, 57], but genetic differentiation also correlates with soil nutrient content and at least four principal components constructed from climatic variables [33].

Origin and timing of introgression If mexicana ancestry found in contemporary maize genomes facilitated maize’s colonization of the highlands approximately 6.2 thousands years ago [36], we would expect introgressed ancestry tracts to be short, due to many generations of recombination, and possibly to be derived from an ancient source population common to many present-day maize populations. To test these predictions, we estimated local ancestry across the genome for individuals from each sympatric maize and mexicana population using a hidden Markov model (HMM) based on read counts ([58]; see Materials and methods). For each admixed population, this HMM simultaneously estimates local ancestry and, by optimizing the transition rate between different (hidden) ancestry states, the generations since admixture. We assumed a 3-way admixture scenario in which a founding mexicana population receives a pulse of parviglumis ancestry, then a pulse of maize ancestry. Admixture between maize and mexicana is generally old, with median estimates of 1014 generations for sympatric maize populations and 509 generations for sympatric mexicana populations (S3 Fig). Parviglumis admixture timing estimates vary substantially across populations (median: 173, range: 29–1006). Because the HMM fits a single-pulse per ancestry to what was almost certainly multiple admixture events over time, we caution against over-interpretation of exact dates. Multiple pulses or ongoing gene flow biases estimates towards the more recent pulse(s) [59, 60] and even old estimates do not exclude the possibility of limited more recent admixture. These single-pulse approximations do, however, provide evidence that a large proportion of the introgression, especially mexicana ancestry into maize, is found on short ancestry tracts and therefore relatively old. To identify likely source population(s) for introgressed ancestry, we compared F ST between all sympatric populations using only reads from high-confidence homozygous ancestry tracts (posterior > 0.8) for maize and mexicana ancestry separately. We find that most mexicana ancestry in maize resembles other mexicana ancestry introgressed into other maize populations, rather that mexicana ancestry from the local sympatric mexicana population (Fig 3). This finding is consistent with most introgressed ancestry being drawn from a communal source population, but none of the sympatric mexicana populations have low enough F ST to tracts introgressed into maize to be a recent source. While we cannot rule out recent introgression from an unsampled source population, the timing of our admixture estimates is more consistent with divergence of mexicana ancestry, once introgressed into a maize background, from its original source population(s) (S3 Fig). Additionally, mexicana ancestry tracts in maize have only slightly reduced genetic diversity (π, S4 Fig), meaning many mexicana haplotypes have introgressed into maize at any given locus, with no evidence of a strong historical bottleneck. PPT PowerPoint slide

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TIFF original image Download: Fig 3. F ST between ancestry tracts from different populations. F ST between each pair of populations for maize ancestry tracts are shown in the upper left triangle, while F ST estimates for mexicana ancestry tracts are shown in the lower right triangle. Populations are sorted by subspecies, then elevation. Local sympatric maize-mexicana population pairs are highlighted with a white dot and do not show reduced F ST relative to other (non-local) maize-mexicana comparisons. Additionally, introgressed mexicana ancestry shows low differentiation between maize populations (creating a light-colored maize block in the left corner of the lower right triangle) and no potential mexicana source populations show especially low F ST with this block. Light coloring generally across the upper left triangle reflects the low differentiation within maize ancestry, providing little information to distinguish between potential maize ancestry sources. https://doi.org/10.1371/journal.pgen.1009810.g003 Two lower elevation maize populations are an exception to this general pattern: Ixtlan and Penjamillo. These populations have higher F ST between their introgressed ancestry tracts and other mexicana tracts in maize (Fig 3), more recent timing of admixture estimates (S3 Fig), and reduced genetic diversity (S4 Fig). These patterns could be caused by small population sizes and more recent independent admixture, although F ST does not identify a likely mexicana source population. Consistent with this interpretation, we have evidence that local maize at Ixtlan is at least partially descended from recently introduced commercial seed (relayed by local farmers [43]). The lack of a clear reduction in F ST for mexicana ancestry tracts between sympatric population pairs, combined with older timing of admixture estimates, indicates that while contemporary hybridization may occur in the field between maize crops and adjacent mexicana populations, this is not the source for the bulk of the introgressed mexicana ancestry segregating in highland maize. Instead, we propose that the majority of mexicana ancestry in maize derives from admixture over 1000 years ago, possibly from a diverse set of mexicana source populations over a large geographic and temporal span, and the resulting ancestry tracts are now distributed across different contemporary maize populations. These genomewide average F ST results, however, do not exclude the possibility that adaptively introgressed haplotypes at a particular locus came from one or more distinct, possibly local, source populations. While we also analyzed F ST within high-confidence maize ancestry tracts, we found that maize ancestry is too homogeneous to make inferences about potential admixture source populations of maize into mexicana (Fig 3 and S4 Fig).

Selection against introgression genomewide When there is widespread selection against introgressing variants at many loci across the genome, selection will more efficiently remove linked ancestry in regions of the genome with lower recombination rates, which creates a positive relationship between local recombination rate and the proportion of introgressed ancestry [4–13, 61]. To test whether such negative selection is shaping patterns of introgression genomewide in sympatric maize and mexicana, we first divided the genome into quintiles based on the local recombination rates for 1 cM windows. We then ran NGSAdmix on the SNPs within each quintile separately, using K = 3 clusters, to estimate ancestry proportions for each quintile. We used a recombination map from maize [62], which is likely to be correlated with other Zea subspecies at least at the level of genomic quintiles. A limitation of this analysis, however, is that we do not have a recombination map for hybrid populations, which means that e.g. segregating structural inversions will not necessarily show low recombination rates. Our results from sympatric maize are consistent with selection against mexicana introgression at many loci genomewide, resulting in lower introgressed ancestry in regions of the genome with lower recombination rates (Fig 4A). We find a positive Spearman’s rank correlation between recombination rate quintile and mean introgressed mexicana ancestry proportion (ρ = 1.00, CI 95 [0.80, 1.00]), reflecting the fact that introgression increases monotonically across quintiles. A similar analysis using f 4 statistics replicates this result (see Materials and methods, S5 and S6 Figs). The higher elevation maize populations show this pattern most starkly; while all individuals have low mexicana ancestry for the lowest recombination rate quintile, some high elevation populations have individuals with over 40% introgressed ancestry for the highest recombination rate quintile (Fig 4B). Using a linear-model fit, we found a significant positive interaction between recombination rate quintile and the slope of ancestry across elevation in sympatric maize (S4 Table). This is again consistent with low-recombination rate regions having a stronger effect of linked selection reducing mexicana ancestry, with higher elevation maize populations either experiencing larger amounts of gene flow or retaining more ancestry due to adaptive processes in high recombination regions. PPT PowerPoint slide

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TIFF original image Download: Fig 4. . (A) Introgressed ancestry by recombination rate. Inferred average genomewide introgressed ancestry in sympatric maize and mexicana individuals (NGSAdmix K = 3), by recombination rate quintiles. Group mean and 95% confidence interval based on bootstrap percentiles (n = 100) are depicted in black. Introgressed ancestry estimates for each individual are shown as points and points are jittered for better visualization. (B) Slope of mexicana ancestry introgressed into maize populations across elevation for each recombination rate quintile, based on NGSAdmix estimates. Each point is a sympatric maize individual and lines show the best-fit linear model for ancestry by elevation (with shaded 95% confidence interval), estimated separately for each quintile. https://doi.org/10.1371/journal.pgen.1009810.g004 Because recombination rate is positively correlated with gene density in Zea [63], we also tested the Spearman’s rank correlation between quintiles defined by coding base pairs per cM and their proportion introgressed mexicana ancestry. Again we found evidence supporting pervasive selection against introgression (S8 Fig, ρ = −1.00, CI 95 [−1.00, −0.90]). In contrast, sympatric mexicana shows an unexpected negative relationship between recombination rate and introgression, with reduced maize ancestry in the highest recombination rate regions of the genome (ρ = −1.00, CI 95 [−1.00, −0.90]). Correlations with coding bp per cM and based on f 4 statistics corroborate this pattern (see S6 Fig). One explanation is that some portion of maize alleles are beneficial in a mexicana background. While maize ancestry in general is not predicted to provide adaptive benefits in teosinte, invasive mexicana in Europe shows selective sweeps for maize ancestry at multiple loci that have contributed to its establishment as a noxious weed [64] and we speculate that maize could be a source of alleles adapted to human-modified landscapes. We repeated these analyses using local ancestry calls as our introgression estimates and found a non-significant Spearman’s rank correlation between mexicana introgression and recombination rates for 1 cM windows in sympatric maize (S9 Fig, ρ = 0.011, CI 95 [−0.038, 0.061]) and a positive rank correlation between maize introgression and recombination rate in sympatric mexicana (ρ = 0.385, CI 95 [0.341, 0.428]). Contrasting results between global and local ancestry methods could be a reflection of true evolutionary differences across different time periods; local ancestry methods capture patterns from more recent gene flow that comes in longer ancestry blocks while STRUCTURE-like algorithms (NGSAdmix) and f 4 statistics are based on allele frequencies that collapse information across ancestry blocks of any size, capturing a longer evolutionary time scale. This interpretation would suggest that mexicana has experienced stronger selection against more recent maize gene flow than historical gene flow. However, we caution that local ancestry methods may also have subtle biases in power that are sensitive to local recombination rates and make them less reliable for comparing ancestry patterns across recombination rate quintiles. Overall, we find support for widespread selection against introgression into maize and mixed results from similar tests of this hypothesis in mexicana.

Genomewide scan for selection on introgressed ancestry We scanned the genome for two types of widespread selection on introgressed ancestry: consistent selection across populations creating an overall excess or deficit of introgression, and fitness trade-offs creating steep clines in mexicana ancestry across elevation. We used our MVN simulated ancestry frequencies to set false-discovery-rates for excess and deficits of mexicana and maize introgression as well as steeper than expected slopes between mexicana ancestry and elevation (see S31 Fig for model fit). We find several regions with high introgression in both directions that are unlikely to be explained by shared demographic history alone (Fig 7A). These regions of adaptive introgression (< 5% FDR) are spread across the genome and cover a small fraction (<0.5%) of the genome in both subspecies. We additionally find evidence of adaptive parviglumis introgression into each subspecies (S32 Fig). We do not have power to determine if individual genes or regions are barriers to introgression because zero introgressed ancestry is not unusual under our simulated neutral model, given both low genomewide introgression and positive ancestry covariance between admixed populations (Fig 7). PPT PowerPoint slide

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TIFF original image Download: Fig 7. Genomewide scan for selection on introgressed ancestry. (A) Mean mexicana ancestry introgressed into sympatric maize populations and mean maize ancestry introgressed into sympatric mexicana populations. (B) Slope of mexicana ancestry proportion over a 1 km elevation gain in sympatric maize and mexicana populations. In both (A) and (B) the blue lines show the 5% false discovery rates, set using multi-variate normal simulations. Positions for Inv4m [50] and the mhl1 locus [65] were converted to the maize reference genome v4 coordinates using Assembly Converter (ensembl.gramene.org). Chromosome numbers are placed at the centromere midpoint (approximate centromere positions are from [66]). https://doi.org/10.1371/journal.pgen.1009810.g007 Additionally, we identify outlier loci across the genome where mexicana ancestry forms steep clines across elevation (Fig 7). Our top candidate for strong associations between introgression and elevation in maize is Inv4m, a large 14 Mb inversion on chromosome 4 previously identified to have introgressed into high elevation maize populations [43–45, 67]. This inversion maintains steep elevational clines within teosintes [50], overlaps QTLs for leaf pigmentation and macrohairs [42], and is associated with increased yield in maize at high elevations and decreased yield at low elevations [67], but has thus far eluded functional characterization of genes within the inversion [67]. Our second strongest association co-localizes with macrohairless1 (mhl1), a locus on chromosome 9 that controls macrohair initiation on the leaf blade [65] and is associated with a major QTL explaining 52% of macrohair variation between high and low elevation teosinte mapping parents [42]. Within teosintes, populations of the lowland ancestor of maize, parviglumis, show convergent soft sweeps at the mhl1 locus not shared by mexicana [32]. Macrohairs are characteristic highland phenotypes in teosinte and maize and are thought to confer adaptive benefits through insect defence and/or thermal insulation [41, 42]. We identified a 3 Mb outlier region within the larger mhl1 QTL which we analyzed further using PCA. We found three genetic clusters along the first principal component, evidence that an inversion polymorphism (hereafter Inv9f) maintains differentiation between maize/parviglumis and mexicana haplotypes across this region (S33 and S34 Figs). Additionally, we found evidence that the mexicana-type allele at the inversion segregates at low frequency within our lowland parviglumis reference population. Based on reduced diversity, the lowland maize/parviglumis-type allele at the inversion is likely derived (S6 Table). Thus mexicana-alleles at Inv9f could have been inherited by maize either through introgression or incomplete lineage sorting before selection pushed them to high frequency in highland populations. The clinal patterns of admixture that we observe at inversions Inv4m and Inv9f suggest they contribute to elevation-based adaptation in maize, with variation in their fitness impacts even within the historic elevational range of mexicana. While our highest peaks localize with regions previously associated with characteristic highland phenotypes, many additional outlier regions with steep increases in mexicana ancestry across elevation have undiscovered associations with local adaptation to elevation. Additionally, outliers for steep ancestry slopes across elevation in sympatric mexicana suggest that introgression from maize into mexicana may facilitate adaptation in mexicana at the lower end of its elevational range.

Selection at candidate domestication genes We hypothesized that domestication genes will be barriers to introgression bilaterally between maize and mexicana [43]. While we do not have power to identify individual outlier genes that have low introgression, we can test for enriched overlap between ‘introgression deserts’ and a set of putative domestication genes spread across the genome. We examined introgression for a sample of 15 well-characterized domestication genes from the literature (see S7 Table), and compared them to the regions of the genome with the lowest 5% introgression of teosinte ancestry into sympatric maize and maize ancestry into sympatric mexicana (‘introgression deserts’). A small but enriched subset of these domestication genes overlap with introgression deserts in sympatric maize (5, P < 0.001) and likewise in sympatric mexicana (5, P = 0.001). Among these 15 domestication genes, we find that teosinte branched1 (tb1), a key transciption factor that regulates branching vs. apical dominance [68, 69], overlaps introgression deserts in both maize and mexicana, consistent with tb1’s role at the top of the domestication regulatory hierarchy [70]. We also find evidence for reduced introgression into both maize and mexicana at teosinte glume architecture1 (tga1) [71, 72], which is associated with ‘naked’ edible grains. Another six domestication genes have low introgression in one direction only [73–77] (see S7 Table). Among these, sugary1 (su1) in the starch pathway has low maize ancestry in mexicana but shows a steep increase in introgressed mexicana ancestry proportion with elevation in maize (+0.95 per km, < 5% FDR), which suggests this gene has pleiotropic effects on non-domestication traits in maize, with fitness trade-offs across elevation. Sugary1 mutations modify the sweetness, nutrient content and texture of maize kernels (e.g. sweet corn), but also affect seed germination and emergence at cold temperatures [78], candidate pleiotropic effects that could be more deleterious at higher elevations. The remaining seven domestication genes do not overlap introgression deserts in either subspecies despite evidence for their roles in domestication: zfl2 (cob rank) [79–81], pbf1 (storage protein synthesis) [82], ba1 (plant architecture) [83], ae1 (starch biosynthesis) [76], ra1 and ra2 (inflorescence architecture) [84, 85] and ZmSh1–5.1+ZmSh1–5.2 (seed shattering) [75]. Despite evidence of introgression at many domestication loci, maize populations retain all of the classic domestication traits, and mexicana populations maintain ‘wild’ forms. Epistasis for domestication traits [47] could help explain this discrepancy if compensatory effects from other loci contribute to maintaining domestication traits in admixed highland maize, or if key domestication alleles segregate at moderate frequencies within mexicana but do not have the same phenotypic effects in a teosinte background.

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