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The genomic signature of crop-wild introgression in maize.

Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J - PLoS Genet. (2013)

Bottom Line: 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.Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of California Davis, Davis, California, United States of America.

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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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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pgen-1003477-g001: Map of collection sites.Light red dots indicate known mexicana populations and larger, dark red dots indicate populations included in the current study.

Mentions: To assess the extent of hybridization and introgression we collected nine sympatric population pairs of maize and mexicana and one allopatric mexicana population from across the highlands of Mexico (Table S1; Figure 1) and genotyped 189 individuals for 39,029 SNPs (see Materials and Methods). Genotype data at the same loci were obtained from Chia et al.[65] for a reference allopatric maize population. Average expected heterozygosity (HE), percent polymorphic loci (%P), and the proportion of privately segregating sites were higher in maize than mexicana (t-test, p≤0.012 for all comparisons, Table S2), likely influenced by the absence of mexicana from the discovery panel used to develop the genotyping platform [66]. However, substantial variation in diversity was observed across populations within taxa (e.g., %P ranged from 52–88% in maize and from 44–79% in mexicana (Table S2)) and meaningful comparisons can be made at this level. Our analysis of diversity identified the Ixtlan maize population as an extreme outlier, containing 31% fewer polymorphic markers than any other maize population. Discussion with farmers during our collection revealed that Ixtlan maize was initially a commercial variety whose seed had been replanted for a number of generations. Excluding this population, diversity in mexicana populations varied much more substantially than in maize (e.g., variance in %P across mexicana populations was 7-fold higher; Table S2)


The genomic signature of crop-wild introgression in maize.

Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J - PLoS Genet. (2013)

Map of collection sites.Light red dots indicate known mexicana populations and larger, dark red dots indicate populations included in the current study.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3649989&req=5

pgen-1003477-g001: Map of collection sites.Light red dots indicate known mexicana populations and larger, dark red dots indicate populations included in the current study.
Mentions: To assess the extent of hybridization and introgression we collected nine sympatric population pairs of maize and mexicana and one allopatric mexicana population from across the highlands of Mexico (Table S1; Figure 1) and genotyped 189 individuals for 39,029 SNPs (see Materials and Methods). Genotype data at the same loci were obtained from Chia et al.[65] for a reference allopatric maize population. Average expected heterozygosity (HE), percent polymorphic loci (%P), and the proportion of privately segregating sites were higher in maize than mexicana (t-test, p≤0.012 for all comparisons, Table S2), likely influenced by the absence of mexicana from the discovery panel used to develop the genotyping platform [66]. However, substantial variation in diversity was observed across populations within taxa (e.g., %P ranged from 52–88% in maize and from 44–79% in mexicana (Table S2)) and meaningful comparisons can be made at this level. Our analysis of diversity identified the Ixtlan maize population as an extreme outlier, containing 31% fewer polymorphic markers than any other maize population. Discussion with farmers during our collection revealed that Ixtlan maize was initially a commercial variety whose seed had been replanted for a number of generations. Excluding this population, diversity in mexicana populations varied much more substantially than in maize (e.g., variance in %P across mexicana populations was 7-fold higher; Table S2)

Bottom Line: 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.Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of California Davis, Davis, California, United States of America.

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.

Show MeSH