The Genomic Signature of Crop-Wild Introgression in Maize

Matthew B. Hufford, Pesach Lubinksy, Tanja Pyhäjärvi and 3 more

PLoS Genetics · 2013

doi:10.1371/journal.pgen.1003477 (opens in a new tab)

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Abstract

The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

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Figures5

From PubMed Central, U.S. National Library of Medicine.

Figure 1
Full legend
Map of collection sites. Light red dots indicate known mexicana populations and larger, dark red dots indicate populations included in the current study.
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Figure 2
Population-level polymorphism and differentiation. (A) Correlation of percent polymorphic loci in sympatric populations of mexicana and maize. (B) Proportion of shared and privately segregating polymorphisms in mexicana and maize and fixed differences between taxa. Letters above bars indicate sympatric maize/mexicana comparisons (S), maize from a given population versus allopatric mexicana (Ax) and mexicana from a given population versus allopatric maize (Az). (C) Pairwise differentiation (FST) in sympatric and allopatric comparisons of mexicana and maize. (D) Bar plot of assignment proportions from STRUCTURE analysis at K = 2 for mexicana (maroon) and maize (gold) individuals. The Ixtlan maize population was excluded from this figure and the STRUCTURE analysis.
Full legend
Population-level polymorphism and differentiation. (A) Correlation of percent polymorphic loci in sympatric populations of mexicana and maize. (B) Proportion of shared and privately segregating polymorphisms in mexicana and maize and fixed differences between taxa. Letters above bars indicate sympatric maize/mexicana comparisons (S), maize from a given population versus allopatric mexicana (Ax) and mexicana from a given population versus allopatric maize (Az). (C) Pairwise differentiation (FST) in sympatric and allopatric comparisons of mexicana and maize. (D) Bar plot of assignment proportions from STRUCTURE analysis at K = 2 for mexicana (maroon) and maize (gold) individuals. The Ixtlan maize population was excluded from this figure and the STRUCTURE analysis.
Open Figure 2 full size (opens in a new tab)

Figure 3
Detection of introgression across chromosome 4. (A) Stacked bar plots of the HAPMIX introgression scan across sympatric populations. Population labels are indicated between plots for maize (gold) and mexicana (maroon). Lighter colors indicate introgression initially detected in each population and darker colors show these values after subtracting introgression proportions from jackknife samples of the allopatric reference populations that may be due to false positives. A dotted black line indicates the position of the centromere. (B) Stacked bar plots of the STRUCTURE introgression scan across sympatric populations. The mexicana group is indicated by maroon and the maize group is indicated by gold. The y-axis for each population in (A) and (B) indicates the average admixture proportion across individuals. (C) Genomic regions in maize populations showing greater than 50% membership in mexicana.
Full legend
Detection of introgression across chromosome 4. (A) Stacked bar plots of the HAPMIX introgression scan across sympatric populations. Population labels are indicated between plots for maize (gold) and mexicana (maroon). Lighter colors indicate introgression initially detected in each population and darker colors show these values after subtracting introgression proportions from jackknife samples of the allopatric reference populations that may be due to false positives. A dotted black line indicates the position of the centromere. (B) Stacked bar plots of the STRUCTURE introgression scan across sympatric populations. The mexicana group is indicated by maroon and the maize group is indicated by gold. The y-axis for each population in (A) and (B) indicates the average admixture proportion across individuals. (C) Genomic regions in maize populations showing greater than 50% membership in mexicana.
Open Figure 3 full size (opens in a new tab)

Figure 4
Growth chamber experiment. (A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.
Full legend
Growth chamber experiment. (A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.
Open Figure 4 full size (opens in a new tab)

Figure 5
Contribution of mexicana germplasm to a global maize diversity panel. (A) The difference between the average IBS proportion with mexicana individuals and the average IBS proportion with parviglumis individuals calculated across six groups of modern maize lines identified by Flint-Garcia et al. [81] in the maize association population. Positive values indicate greater IBS with mexicana. (B) Average IBS across chromosome 3 in each line in the maize association population compared to both mexicana and parviglumis. The one-to-one line is indicated by the dashed line. Colors are as in Figure 5A. (C) The proportion of sites across the genome showing greater IBS with mexicana than with parviglumis for each of the six maize association population groups.
Full legend
Contribution of mexicana germplasm to a global maize diversity panel. (A) The difference between the average IBS proportion with mexicana individuals and the average IBS proportion with parviglumis individuals calculated across six groups of modern maize lines identified by Flint-Garcia et al. [81] in the maize association population. Positive values indicate greater IBS with mexicana. (B) Average IBS across chromosome 3 in each line in the maize association population compared to both mexicana and parviglumis. The one-to-one line is indicated by the dashed line. Colors are as in Figure 5A. (C) The proportion of sites across the genome showing greater IBS with mexicana than with parviglumis for each of the six maize association population groups.
Open Figure 5 full size (opens in a new tab)

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