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)

Read free

We email you when a new notice or a question about this paper appears.

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.

No text here

Its licence does not allow us to show the full text. Read it at PubMed Central:

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.
Open Figure 1 full size (opens in a new tab)

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)

References99

1.
Stebbins GL (1959 ) The role of hybridization in evolution. P Am Philos Soc 103: 231–251.
Not in our library
2.
Anderson E (1948 ) Hybridization of the habitat. Evolution 2: 1–9.
Not in our library
3.
Anderson E, Stebbins GL (1954 ) Hybridization as an evolutionary stimulus. Evolution 8: 378–388.
Not in our library
4.
Arnold ML (2004 ) Transfer and origin of adaptations through natural hybridization: Were Anderson and Stebbins right? Plant Cell 16: 562–570.
Not in our library10.1105/tpc.histpersp (opens in a new tab)
5.
Arnold ML, Martin NH (2010 ) Hybrid fitness across time and habitats. Trends Ecol Evol 25: 530–536.
Not in our library10.1016/j.tree.2010.06.005 (opens in a new tab)
6.
Arnold ML (2004 ) Natural hybridization and the evolution of domesticated, pest and disease organisms. Mol Ecol 13: 997–1007.
Not in our library10.1111/j.1365-294x.2004.02145.x (opens in a new tab)
7.
Ellstrand NC, Heredia SM, Leak-Garcia JA, Heraty JM, Burger JC, et al (2010 ) Crops gone wild: evolution of weeds and invasives from domesticated ancestors. Evol Appl 3: 494–504.
Not in our library10.1111/j.1752-4571.2010.00140.x (opens in a new tab)
8.
Grant BR, Grant PR (1996 ) High survival of Darwin's finch hybrids: Effects of beak morphology and diets. Ecology 77: 500–509.
Not in our library
9.
Grant PR, Grant BR (2010 ) Conspecific versus heterospecific gene exchange between populations of Darwin's finches. Philos T Roy Soc B 365: 1065–1076.
Not in our library10.1098/rstb.2009.0283 (opens in a new tab)
10.
Whitney KD, Randell RA, Rieseberg LH (2006 ) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am Nat 167: 794–807.
Not in our library10.1086/504606 (opens in a new tab)
11.
Whitney KD, Randell RA, Rieseberg LH (2010 ) Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 187: 230–239.
Not in our library10.1111/j.1469-8137.2010.03234.x (opens in a new tab)
12.
Heiser CB (1951 ) Hybridization in the annual sunflowers - Helianthus-annuusXH-debilis var-cucumerifolius. Evolution 5: 42–51.
Not in our library
13.
Kim SC, Rieseberg LH (1999 ) Genetic architecture of species differences in annual sunflowers: Implications for adaptive trait introgression. Genetics 153: 965–977.
Not in our library10.1093/genetics/153.2.965 (opens in a new tab)
14.
Kim M, Cui M-L, Cubas P, Gillies A, Lee K, et al (2008 ) Regulatory genes control a key morphological and ecological trait transferred between species. Science 322: 1116–1119.
Not in our library10.1126/science.1164371 (opens in a new tab)
15.
Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A, et al (2012 ) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94–98.
Not in our library10.1038/nature11041 (opens in a new tab)
16.
Adaptive Introgression across Species Boundaries in Heliconius Butterflies · 2012
17.
Durand EY, Patterson N, Reich D, Slatkin M (2011 ) Testing for ancient admixture between closely related populations. Mol Biol Evol 28: 2239–2252.
Not in our library10.1093/molbev/msr048 (opens in a new tab)
18.
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, et al (2010 ) A draft sequence of the Neandertal genome. Science 328: 710–722.
Not in our library10.1126/science.1188021 (opens in a new tab)
19.
Two Evolutionary Histories in the Genome of Rice: the Roles of Domestication Genes · 2011
20.
The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing · 2009
21.
Reich D, Green RE, Kircher M, Krause J, Patterson N, et al (2010 ) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053–1060.
Not in our library10.1038/nature09710 (opens in a new tab)
22.
Sun Y, Corcoran P, Menkis A, Whittle CA, Andersson SGE, et al (2012 ) Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma. PLoS Genet 8: e1002820 doi:10.1371/journal.pgen.1002820.
Not in our library10.1371/journal.pgen.1002820 (opens in a new tab)
23.
Arnaud JF, Viard F, Delescluse M, Cuguen J (2003 ) Evidence for gene flow via seed dispersal from crop to wild relatives in Beta vulgaris (Chenopodiaceae): consequences for the release of genetically modified crop species with weedy lineages. P Roy Soc Lond B Bio 270: 1565–1571.
Not in our library10.1098/rspb.2003.2407 (opens in a new tab)
24.
Ellstrand NC (2003) Dangerous Liaisons? When Cultivated Plants Mate with Their Wild Relatives. Baltimore, Maryland: The Johns Hopkins University Press. 244 p.
Not in our library
25.
Gutierrez A, Cantamutto M, Poverene M (2011 ) Persistence of sunflower crop traits and fitness in Helianthus petiolaris populations. Plant Biol 13: 821–830.
Not in our library10.1111/j.1438-8677.2010.00433.x (opens in a new tab)
26.
Morrell PL, Williams-Coplin TD, Lattu AL, Bowers JE, Chandler JM, et al (2005 ) Crop-to-weed introgression has impacted allelic composition of johnsongrass populations with and without recent exposure to cultivated sorghum. Mol Ecol 14: 2143–2154.
Not in our library10.1111/j.1365-294x.2005.02579.x (opens in a new tab)
27.
Xia HB, Wang W, Xia H, Zhao W, Lu BR (2011 ) Conspecific crop-weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS ONE 6: e16189 doi:10.1371/journal.pone.0016189.
Not in our library10.1371/journal.pone.0016189 (opens in a new tab)
28.
Fujino K, Wu J, Sekiguchi H, Ito T, Izawa T, et al (2010 ) Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. Mol Genet Genomics 284: 137–146.
Not in our library10.1007/s00438-010-0555-2 (opens in a new tab)
29.
McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, et al (2009 ) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. P Natl Acad Sci USA 106: 12273–12278.
Not in our library10.1073/pnas.0900992106 (opens in a new tab)
30.
Genomic Diversity and Introgression in O. sativa Reveal the Impact of Domestication and Breeding on the Rice Genome · 2010
31.
New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties · 2012
32.
Luo MC, Yang ZL, You FM, Kawahara T, Waines JG, et al (2007 ) The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor Appl Genet 114: 947–959.
Not in our library10.1007/s00122-006-0474-0 (opens in a new tab)
33.
Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, et al (2011 ) Genetic structure and domestication history of the grape. P Natl Acad Sci USA 108: 3530–3535.
Not in our library10.1073/pnas.1009363108 (opens in a new tab)
34.
Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, et al (2002 ) A single domestication for maize shown by multilocus microsatellite genotyping. P Natl Acad Sci USA 99: 6080–6084.
Not in our library10.1073/pnas.052125199 (opens in a new tab)
35.
Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R (2009 ) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. P Natl Acad Sci USA 106: 5019–5024.
Not in our library10.1073/pnas.0812525106 (opens in a new tab)
36.
van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM, et al (2011 ) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. P Natl Acad Sci USA 108: 1088–1092.
Not in our library10.1073/pnas.1013011108 (opens in a new tab)
37.
Vigouroux Y, Glaubitz JC, Matsuoka Y, Goodman MM, Jesus SG, et al (2008 ) Population structure and genetic diversity of New World maize races assessed by DNA microsatellites. Am J Bot 95: 1240–1253.
Not in our library10.3732/ajb.0800097 (opens in a new tab)
38.
Hufford MB, Martinez-Meyer E, Gaut BS, Eguiarte LE, Tenaillon MI (2012 ) Past and present distributions of wild and domesticated Zea mays: a chance to revisit maize history. PLoS ONE 7: e47659 doi:10.1371/journal.pone.0047659.
Not in our library10.1371/journal.pone.0047659 (opens in a new tab)
39.
Ross-Ibarra J, Tenaillon M, Gaut BS (2009 ) Historical divergence and gene flow in the genus Zea. Genetics 181: 1397–1409.
Not in our library10.1534/genetics.108.097238 (opens in a new tab)
40.
Wilkes HG (1967) Teosinte: The Closest Relative of Maize. Cambridge, Massachusetts: The Bussey Institute of Harvard University. 159 p.
Not in our library
41.
Wilkes HG (1977 ) Hybridization of maize and teosinte, in Mexico and Guatemala and improvement of maize. Econ Bot 31: 254–293.
Not in our library
42.
Lauter N, Gustus C, Westerbergh A, Doebley J (2004 ) The inheritance and evolution of leaf pigmentation and pubescence in teosinte. Genetics 167: 1949–1959.
Not in our library10.1534/genetics.104.026997 (opens in a new tab)
43.
Barthakur N (1974 ) Temperature differences between two pigmented types of corn plants. Int J Biometeorol 18: 70–75.
Not in our library
44.
Collins GN (1921 ) Teosinte in Mexico - The closest wild relative of maize is teosinte - a forage plant hitherto known only as an annual. A perennial form discovered in southern Mexico should prove of value to the breeder. J Hered 12: 339–350.
Not in our library
45.
Doebley JF (1984 ) Maize introgression into teosinte - a reappraisal. Ann Mo Bot Gard 71: 1100–1113.
Not in our library
46.
Doebley J (1990 ) Molecular evidence and the evolution of maize. Econ Bot 44: 6–27.
Not in our library
47.
Rodriguez JG, Sanchez JJ, Baltazar B, De la Cruz L, Santacruz-Ruvalcaba F, et al (2006 ) Characterization of floral morphology and synchrony among Zea species in Mexico. Maydica 51: 383–398.
Not in our library
48.
Evans MMS, Kermicle JL (2001 ) Teosinte crossing barrier1, a locus governing hybridization of teosinte with maize. Theor Appl Genet 103: 259–265.
Not in our library
49.
Kermicle JL, Evans MMS (2010 ) The Zea mays sexual compatibility gene ga2: naturally occurring alleles, their distribution, and role in reproductive isolation. J Hered 101: 737–749.
Not in our library10.1093/jhered/esq090 (opens in a new tab)
50.
Kermicle JL, Taba S, Evans MMS (2006 ) The gametophyte-1 locus and reproductive isolation among Zea mays subspecies. Maydica 51: 219–225.
Not in our library
51.
Baltazar BM, Sanchez-Gonzalez JD, de la Cruz-Larios L, Schoper JB (2005 ) Pollination between maize and teosinte: an important determinant of gene flow in Mexico. Theor Appl Genet 110: 519–526.
Not in our library10.1007/s00122-004-1859-6 (opens in a new tab)
52.
Ellstrand NC, Garner LC, Hegde S, Guadagnuolo R, Blancas L (2007 ) Spontaneous hybridization between maize and teosinte. J Hered 98: 183–187.
Not in our library10.1093/jhered/esm002 (opens in a new tab)
53.
Barton NH (2001 ) The role of hybridization in evolution. Mol Ecol 10: 551–568.
Not in our library10.1046/j.1365-294x.2001.01216.x (opens in a new tab)
54.
Mallet J (2005 ) Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229–237.
Not in our library10.1016/j.tree.2005.02.010 (opens in a new tab)
55.
Doebley J, Goodman MM, Stuber CW (1987 ) Patterns of isozyme variation between maize and Mexican annual teosinte. Econ Bot 41: 234–246.
Not in our library
56.
Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter M, et al (2004 ) The role of barren stalk1 in the architecture of maize. Nature 432: 630–635.
Not in our library10.1038/nature03148 (opens in a new tab)
57.
Warburton ML, Wilkes G, Taba S, Charcosset A, Mir C, et al (2011 ) Gene flow among different teosinte taxa and into the domesticated maize gene pool. Genet Resour Crop Ev 58: 1243–1261.
Not in our library
58.
Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez J, et al (2005 ) Genetic diversity and population structure of teosinte. Genetics 169: 2241–2254.
Not in our library10.1534/genetics.104.031393 (opens in a new tab)
59.
Delplancke M, Alvarez N, Espindola A, Joly H, Benoit L, et al (2012 ) Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evol Appl 5: 317–329.
Not in our library10.1111/j.1752-4571.2011.00223.x (opens in a new tab)
60.
Huebner S, Guenther T, Flavell A, Fridman E, Graner A, et al (2012 ) Islands and streams: clusters and gene flow in wild barley populations from the Levant. Mol Ecol 21: 1115–1129.
Not in our library10.1111/j.1365-294x.2011.05434.x (opens in a new tab)
61.
Li Z, Zou J, Mao K, Lin K, Li H, et al (2012 ) Population genetic evidence for complex evolutionary histories of four high altitude juniper species in the Qinghai-Tibetan plateau. Evolution 66: 831–845.
Not in our library10.1111/j.1558-5646.2011.01466.x (opens in a new tab)
62.
Scascitelli M, Whitney KD, Randell RA, King M, Buerkle CA, et al (2010 ) Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation. Mol Ecol 19: 521–541.
Not in our library10.1111/j.1365-294x.2009.04504.x (opens in a new tab)
63.
Baack EJ, Rieseberg LH (2007 ) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17: 513–518.
Not in our library10.1016/j.gde.2007.09.001 (opens in a new tab)
64.
Twyford AD, Ennos RA (2012 ) Next-generation hybridization and introgression. Heredity 108: 179–189.
Not in our library10.1038/hdy.2011.68 (opens in a new tab)
65.
Chia J-M, Song C, Bradbury PJ, Costich D, de Leon N, et al (2012 ) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44: 803–807.
Not in our library10.1038/ng.2313 (opens in a new tab)
66.
A Large Maize (Zea mays L.) SNP Genotyping Array: Development and Germplasm Genotyping, and Genetic Mapping to Compare with the B73 Reference Genome · 2011
67.
Reich D, Kumarasamy T, Patterson N, Price AL, Singh L (2009 ) Reconstructing Indian population history. Nature 461: 489–494.
Not in our library10.1038/nature08365 (opens in a new tab)
68.
Sensitive Detection of Chromosomal Segments of Distinct Ancestry in Admixed Populations · 2009
69.
Falush D, Stephens M, Pritchard JK (2003 ) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567–1587.
Not in our library10.1093/genetics/164.4.1567 (opens in a new tab)
70.
Pritchard JK, Stephens M, Donnelly P (2000 ) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
Not in our library10.1093/genetics/155.2.945 (opens in a new tab)
71.
Hufford MB, Xu X, van Heerwaarden J, Pyhäjärvi T, Chia J-M, et al (2012 ) Comparative population genomics of maize domestication and improvement. Nat Genet 808–811.
Not in our library10.1038/ng.2309 (opens in a new tab)
72.
Whipple CJ, Kebrom TH, Weber AL, Yang F, Hall D, et al (2011 ) grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. P Natl Acad Sci USA 108: E506–E512.
Not in our library10.1073/pnas.1102819108 (opens in a new tab)
73.
From many, one: genetic control of prolificacy during maize domestication. · 2013
Not checked
74.
Doebley J, Stec A, Hubbard L (1997 ) The evolution of apical dominance in maize. Nature 386: 485–488.
Not in our library10.1038/386485a0 (opens in a new tab)
75.
Wang H, Nussbaum-Wagler T, Li BL, Zhao Q, Vigouroux Y, et al (2005 ) The origin of the naked grains of maize. Nature 436: 714–719.
Not in our library10.1038/nature03863 (opens in a new tab)
76.
Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES (2002 ) Genetic diversity and selection in the maize starch pathway. P Natl Acad Sci USA 99: 12959–12962.
Not in our library10.1073/pnas.202476999 (opens in a new tab)
77.
Coop G, Witonsky D, Di Rienzo A, Pritchard JK (2010 ) Using environmental correlations to identify loci underlying local adaptation. Genetics 185: 1411–1423.
Not in our library10.1534/genetics.110.114819 (opens in a new tab)
78.
Pyhäjärvi T, Hufford MB, Mezmouk S, Ross-Ibarra J (2012) Complex patterns of local adaptation in teosinte. arXiv:1208.0634v1. Available at: http://arxiv.org/abs/1208.0634. Accessed 28 February 2013.
Not in our library10.1093/gbe/evt109 (opens in a new tab)
79.
Moose SP, Lauter N, Carlson SR (2004 ) The maize macrohairless1 locus specifically promotes leaf blade macrohair initiation and responds to factors regulating leaf identity. Genetics 166: 1451–1461.
Not in our library10.1534/genetics.166.3.1451 (opens in a new tab)
80.
Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, et al (2012 ) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158: 824–834.
Not in our library10.1104/pp.111.185033 (opens in a new tab)
81.
Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, et al (2005 ) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44: 1054–1064.
Not in our library10.1111/j.1365-313x.2005.02591.x (opens in a new tab)
82.
Gusev A, Lowe JK, Stoffel M, Daly MJ, Altshuler D, et al (2009 ) Whole population, genome-wide mapping of hidden relatedness. Genome Res 19: 318–326.
Not in our library10.1101/gr.081398.108 (opens in a new tab)
83.
Sanchez-Velasquez LR, Ezcurra E, Martinez-Ramos M, Alvarez-Buylla E, Lorente R (2002 ) Population dynamics of Zea diploperennis, an endangered perennial herb: effect of slash and burn practice. J Ecol 90: 684–692.
Not in our library
84.
Freitas FO, Bendel G, Allaby RG, Brown TA (2003 ) DNA from primitive maize landraces and archaeological remains: implications for the domestication of maize and its expansion into South America. J Archaeol Sci 30: 901–908.
Not in our library
85.
Molina J, Sikora M, Garud N, Flowers JM, Rubinstein S, et al (2011 ) Molecular evidence for a single evolutionary origin of domesticated rice. P Natl Acad Sci USA 108: 8351–8356.
Not in our library10.1073/pnas.1104686108 (opens in a new tab)
86.
Badr A, Muller K, Schafer-Pregl R, El Rabey H, Effgen S, et al (2000 ) On the origin and domestication history of barley (Hordeum vulgare). Mol Biol Evol 17: 499–510.
Not in our library10.1093/oxfordjournals.molbev.a026330 (opens in a new tab)
87.
Morrell PL, Clegg MT (2007 ) Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. P Natl Acad Sci USA 104: 3289–3294.
Not in our library10.1073/pnas.0611377104 (opens in a new tab)
88.
Kwak M, Kami JA, Gepts P (2009 ) The putative Mesoamerican domestication center of Phaseolus vulgaris is located in the Lerma-Santiago Basin of Mexico. Crop Sci 49: 554–563.
Not in our library
89.
Heun M, SchaferPregl R, Klawan D, Castagna R, Accerbi M, et al (1997 ) Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278: 1312–1314.
Not in our library
90.
Currat M, Ruedi M, Petit RJ, Excoffier L (2008 ) The hidden side of invasions: Massive introgression by local genes. Evolution 62: 1908–1920.
Not in our library10.1111/j.1558-5646.2008.00413.x (opens in a new tab)
91.
Excoffier L, Foll M, Petit RJ (2009 ) Genetic consequences of range expansions. Annu Rev Ecol Evol S 40: 481–501.
Not in our library
92.
Gavrilets S (1997 ) Hybrid zones with Dobzhansky-type epistatic selection. Evolution 51: 1027–1035.
Not in our library10.1111/j.1558-5646.1997.tb03949.x (opens in a new tab)
93.
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984 ) Ribosomal DNA spacer-length polymorphisms in barley - Mendelian inheritance, chromosomal location, and population-dynamics. P Natl Acad Sci USA 81: 8014–8018.
Not in our library10.1073/pnas.81.24.8014 (opens in a new tab)
94.
R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Not in our library
95.
Thornton K (2003 ) libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19: 2325–2327.
Not in our library10.1093/bioinformatics/btg316 (opens in a new tab)
96.
Weir BS, Cockerham CC (1984 ) Estimating F-statistics for the analysis of population-structure. Evolution 38: 1358–1370.
Not in our library10.1111/j.1558-5646.1984.tb05657.x (opens in a new tab)
97.
Goudet J (2005 ) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5: 184–186.
Not in our library
98.
Lee M, Sharopova N, Beavis WD, Grant D, Katt M, et al (2002 ) Expanding the genetic map of maize with the intermated B73×Mo17 (IBM) population. Plant Mol Biol 48: 453–461.
Not in our library10.1023/a:1014893521186 (opens in a new tab)
99.
Scheet P, Stephens M (2006 ) A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78: 629–644.
Not in our library10.1086/502802 (opens in a new tab)

Cited by papers we hold9

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.