Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH FRONT

Investigation of the domestication of common bean (Phaseolus vulgaris) using multilocus sequence data

Sujan Mamidi A D E , Monica Rossi B , Deepti Annam C , Samira Moghaddam A D , Rian Lee A D , Roberto Papa B and Phillip McClean A D
+ Author Affiliations
- Author Affiliations

A North Dakota State University, Department of Plant Sciences, Fargo, ND 58102, USA.

B Università Politecnica delle Marche, Scienze Ambientali e delle Produzioni Vegetali, Ancona, Italy.

C North Dakota State University, Department of Statistics, Fargo, ND 58102, USA.

D North Dakota State University, Genomics and Bioinformatics Program, Fargo, ND 58102, USA.

E Corresponding author. Emails: sujan_vnv@yahoo.com, sujan.mamidi@gmail.com

Functional Plant Biology 38(12) 953-967 https://doi.org/10.1071/FP11124
Submitted: 21 May 2011  Accepted: 15 September 2011   Published: 7 November 2011

Abstract

Multilocus sequence data collected from domesticated and related wild relatives provides a rich source of information on the effect of human selection on the diversity and adaptability of a species to complex environments. To evaluate the domestication history of common bean (Phaseolus vulgaris L.), multilocus sequence data from landraces representing the various races within the Middle American (MA) and Andean gene pools was evaluated. Across 13 loci, nucleotide diversity was similar between landraces and wild germplasm in both gene pools. The diversity data were evaluated using the approximate Bayesian computation approach to test multiple domestication models and estimate population demographic parameters. A model with a single domestication event coupled with bidirectional migration between wild and domesticated genotypes fitted the data better than models consisting of two or three domestication events in each genepool. The effective bottleneck population size was ~50% of the base population in each genepool. The bottleneck began ~8200 and ~8500 years before present and ended at ~6300 and ~7000 years before present in MA and Andean gene pools respectively. Linkage disequilibrium decayed to a greater extent in the MA genepool. Given the (1) geographical adaptation bottleneck in each wild gene pool, (2) a subsequent domestication bottleneck within each gene pool, (3) differentiation into gene-pool specific races and (4) variable extents of linkage disequilibrium, association mapping experiments for common bean would more appropriately be performed within each genepool.

Additional keywords: ABC approach, association mapping, bottleneck, demography, genepools, linkage disequilibrium, races.


References

Batini C, Lopes J, Behar DM, Calafell F, Jorde LB, van der Veen L, Quintana-Murci L, Spedini G, Destro-Bisol G, Comas D (2011) Insights into the demographic history of African pygmies from complete mitochondrial genomes. Molecular Biology and Evolution 28, 1099–1110.
Insights into the demographic history of African pygmies from complete mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVSrtw%3D%3D&md5=ed0e3531a4c54e3bbae9e6839cb129d9CAS |

Becerra Velasquez VL, Gepts P (1994) RFLP diversity of common bean (Phaseolus vulgaris) in its centers of origin. Genome 37, 256–263.
RFLP diversity of common bean (Phaseolus vulgaris) in its centers of origin.Crossref | GoogleScholarGoogle Scholar |

Beebe S, Skroch PW, Tohme J, Duque MC, Pedraza F, Nienhuis J (2000) Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Science 40, 264–273.
Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD.Crossref | GoogleScholarGoogle Scholar |

Beebe S, Rengifo J, Gaitan E, Duque MC, Tohme J (2001) Diversity and origin of Andean landraces of common bean. Crop Science 41, 854–862.
Diversity and origin of Andean landraces of common bean.Crossref | GoogleScholarGoogle Scholar |

Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Molecular Ecology 19, 2609–2625.
ABC as a flexible framework to estimate demography over space and time: some cons, many pros.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnnvVKgug%3D%3D&md5=4618014a82d4d243f5c23473dd43b410CAS |

Blair MW, Iriarte G, Beebe S (2006) QTL analysis of yield traits in an advanced backcross population derived from a cultivated Andean × wild common bean (Phaseolus vulgaris L.) cross. Theoretical and Applied Genetics 112, 1149–1163.
QTL analysis of yield traits in an advanced backcross population derived from a cultivated Andean × wild common bean (Phaseolus vulgaris L.) cross.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVSmtrY%3D&md5=8a82958b76059e2f8b63963e070f101bCAS |

Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLOS Genetics 6, e1000940
Linkage and association mapping of Arabidopsis thaliana flowering time in nature.Crossref | GoogleScholarGoogle Scholar |

Brady L, Bassett MJ, McClean PE (1998) Molecular markers associated with T and Z, two genes controlling partly coloured seed coat patterns in common bean. Crop Science 38, 1073–1075.
Molecular markers associated with T and Z, two genes controlling partly coloured seed coat patterns in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvFWktrY%3D&md5=06cd4c8aa6fc53ee22193fe85b5de879CAS |

Brown CH (2006) Prehistoric chronology of the common bean in the New World: the linguistic evidence. American Anthropologist 108, 507–516.
Prehistoric chronology of the common bean in the New World: the linguistic evidence.Crossref | GoogleScholarGoogle Scholar |

Buckler ES, Thornsberry JM, Kresovich S (2001) Molecular diversity, structure and domestication of grasses. Genetical Research 77, 213–218.
Molecular diversity, structure and domestication of grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVKit7c%3D&md5=d0791bf143dcf0c025c7852d281f2bd0CAS |

Burkart A, Brücher H (1953) Phaseolus aborigineus Burkart, die mutmassliche andine Stammform der Kulturbohne. Züchter 23, 65–72.

Burke JM, Burger JC, Chapman MA (2007) Crop evolution: from genetics to genomics. Current Opinion in Genetics & Development 17, 525–532.
Crop evolution: from genetics to genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWisbzL&md5=4a5fd64b99358806764da649ffdf4795CAS |

Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Fledel-Alon A, York TL, Polato NR, Olsen KM, Nielsen R, McCouch SR, Bustamante CD, Purugganan MD (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLOS Genetics 3, e163
Genome-wide patterns of nucleotide polymorphism in domesticated rice.Crossref | GoogleScholarGoogle Scholar |

Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172, 557–567.
Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvV2jt7s%3D&md5=69a231ea73151a18ab7a699499435165CAS |

Cardon LR, Palmer LJ (2003) Population structure and spurious associations. Lancet 361, 598–604.
Population structure and spurious associations.Crossref | GoogleScholarGoogle Scholar |

Cattan-Toupance I, Michalakis Y, Neema C (1998) Genetic structure of wild bean populations in their South-Andean centre of origin. Theoretical and Applied Genetics 96, 844–851.
Genetic structure of wild bean populations in their South-Andean centre of origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFSiu74%3D&md5=693d70315fc72208df0fc49c14a27a7cCAS |

Chacón S, Pickersgill B, Debouck DG (2005) Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theoretical and Applied Genetics 110, 432–444.
Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races.Crossref | GoogleScholarGoogle Scholar |

Clark RM, Linton E, Messing J, Doebley JF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. Proceedings of the National Academy of Sciences of the United States of America 101, 700–707.
Pattern of diversity in the genomic region near the maize domestication gene tb1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVWhtbo%3D&md5=920c6fb1fb5cd4141a4d485c932f9ee6CAS |

Csilléry K, Blum MGB, Gaggiotti OE, François O (2010) Approximate Bayesian computation (ABC) in practice. Trends in Ecology & Evolution 25, 410–418.
Approximate Bayesian computation (ABC) in practice.Crossref | GoogleScholarGoogle Scholar |

Debouck DG, Toro O, Paredes OM, Johnson WC, Gepts P (1993) Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northwestern South America. Economic Botany 47, 408–423.
Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northwestern South America.Crossref | GoogleScholarGoogle Scholar |

Depaulis F, Mousset S, Veuille M (2003) Power of neutrality tests to detect bottlenecks and hitchhiking. Journal of Molecular Evolution 57, S190–S200.
Power of neutrality tests to detect bottlenecks and hitchhiking.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsVeiuw%3D%3D&md5=0af1bfbfa8dd1d3bcbdec65ab4c0adafCAS |

Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707.
Evolution, consequences and future of plant and animal domestication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVyltbY%3D&md5=e97ace3dbf7feb36b4c01a382c443227CAS |

Díaz LM, Blair MW (2006) Race structure within the Mesoamerican gene pool of common bean (Phaseolus vulgaris L.) as determined by microsatellite markers. Theoretical and Applied Genetics 114, 143–154.
Race structure within the Mesoamerican gene pool of common bean (Phaseolus vulgaris L.) as determined by microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251–1266.
Inference of bacterial microevolution using multilocus sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltFKhs7k%3D&md5=8bdb64fbcb83dff0e647dc8f8b9a34beCAS |

Doebley J (2004) The genetics of maize evolution. Annual Review of Genetics 38, 37–59.
The genetics of maize evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlOqsg%3D%3D&md5=3644b31daeeeb91dc5c0cacf2a185f72CAS |

Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127, 1309–1321.
The molecular genetics of crop domestication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVyluw%3D%3D&md5=b7feb0b18fa40f4c318b72526193b847CAS |

Ellstrand NC, Schierenbeck KA (2000) Hybridisation as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences of the United States of America 97, 7043–7050.
Hybridisation as a stimulus for the evolution of invasiveness in plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksVKisbk%3D&md5=fc14ea83c28d05277214c9cc100cc927CAS |

Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology Evolution and Systematics 30, 539–563.
Gene flow and introgression from domesticated plants into their wild relatives.Crossref | GoogleScholarGoogle Scholar |

Estoup A, Beaumont M, Sennedot F, Moritz C, Cornuet JM (2004) Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad, Bufo marinus. Evolution 58, 2021–2036.

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=5aede1df804e28ef81e7c9a92a5b45afCAS |

Evans A (1976) Beans. In ‘Evolution of crops plants’. (Ed. J Smartt, NW Simmonds) pp. 168–172. (Longman: London)

Eyre-Walker A, Gaut RL, Hilton H, Feldman DL, Gaut BS (1998) Investigation of the bottleneck leading to the domestication of maize. Proceedings of the National Academy of Sciences of the United States of America 95, 4441–4446.
Investigation of the bottleneck leading to the domestication of maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXis1Ogsr4%3D&md5=28432e0a918cff99abd26282b55f5602CAS |

Fagundes NJR, Ray N, Beaumont M, Neuenschwander S, Salzano FM, Bonatto SL, Excoffier L (2007) Statistical evaluation of alternative models of human evolution. Proceedings of the National Academy of Sciences of the United States of America 104, 17614–17619.
Statistical evaluation of alternative models of human evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12msbjL&md5=6a727f05b1223ef5dfc3a4cc25836378CAS |

Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annual Review of Plant Biology 54, 357–374.
Structure of linkage disequilibrium in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFSgu7c%3D&md5=fa18b79c7b1d5cb4cc6db1a108465bbdCAS |

François O, Blum MGB, Jakobsson M, Rosenberg NA (2008) Demographic history of European populations of Arabidopsis thaliana. PLOS Genetics 4, e1000075
Demographic history of European populations of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Freyre R, Ríos R, Guzmán L, Debouck DG, Gepts P (1996) Ecogeographic distribution of Phaseolus spp. (Fabaceae) in Bolivia. Economic Botany 50, 195–215.
Ecogeographic distribution of Phaseolus spp. (Fabaceae) in Bolivia.Crossref | GoogleScholarGoogle Scholar |

Fuller DQ (2007) Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Annals of Botany 100, 903–924.
Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World.Crossref | GoogleScholarGoogle Scholar |

Galván MZ, Aulicino MB, García Medina S, Balatti PA (2001) Genetic diversity among Northwestern Argentinian cultivars of common bean (Phaseolus vulgaris L.) as revealed by RAPD markers. Genetic Resources and Crop Evolution 48, 251–260.
Genetic diversity among Northwestern Argentinian cultivars of common bean (Phaseolus vulgaris L.) as revealed by RAPD markers.Crossref | GoogleScholarGoogle Scholar |

Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165, 759–769.

Gepts P (1988) Phaseolin as an evolutionary marker. In ‘Genetic resources of Phaseolus beans’. (Ed. P Gepts) pp. 215–241. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Gepts P (1990) Biochemical evidence bearing on the domestication of Phaseolus (Fabaceae) beans. Economic Botany 44, 28–38.
Biochemical evidence bearing on the domestication of Phaseolus (Fabaceae) beans.Crossref | GoogleScholarGoogle Scholar |

Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33, 1124–1130.

Gepts P, Bliss FA (1986) Phaseolin variability among wild and cultivated common beans (Phaseolus vulgaris) from Colombia. Economic Botany 40, 469–478.
Phaseolin variability among wild and cultivated common beans (Phaseolus vulgaris) from Colombia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFyksQ%3D%3D&md5=b83bcb14adfe0abd5ee0b4762a41ae06CAS |

Gepts P, Debouck D (1991) Origin, domestication and evolution of the common bean (Phaseolus vulgaris L.). In ‘Common beans: research for crop improvement’. (Eds A Van Schoonhoven, O Voysest) pp. 7–53. (CAB International: Wallingford, UK)

Gepts P, Osborn TC, Rashka K, Bliss FA (1986) Phaseolin-protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication. Economic Botany 40, 451–468.
Phaseolin-protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFyksA%3D%3D&md5=414bdf1a96212cd3d881dde43030f4a8CAS |

Gepts P, Aragão FJL, de Barros E, Blair MW, Brondani R, Broughton W, Galasso I, Hernández G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sánchez F, Sparvoli F, Yu K (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In ‘Genomics of tropical crop plants’. (Ed. PH Moore, R Ming) pp. 113–143. (Springer: New York)

Glémin S, Bataillon T (2009) A comparative view of the evolution of grasses under domestication. New Phytologist 183, 273–290.
A comparative view of the evolution of grasses under domestication.Crossref | GoogleScholarGoogle Scholar |

Graham P, Vance C (2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872–877.
Legumes: importance and constraints to greater use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFemtb4%3D&md5=3ff6999509d179d807ee0c3cd336fa4bCAS |

Guo J, Wang Y, Song C, Zhou J, Qiu L, Huang H, Wang Y (2010) A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences. Annals of Botany 106, 505–514.
A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGru7%2FK&md5=e27c563eee563818a0abde5b0867739aCAS |

Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Molecular Biology 57, 461–485.
Linkage disequilibrium and association studies in higher plants: present status and future prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtV2gsrk%3D&md5=6058fa6875f77d5135718d6bb2caf542CAS |

Hamblin MT, Casa AM, Sun H, Murray SC, Paterson AH, Aquadro CF, Kresovich S (2006) Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor. Genetics 173, 953–964.
Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xns12qsb4%3D&md5=be00034bd6d4845e5f739176bf21e4c3CAS |

Hamblin MT, Buckler ES, Jannink JL (2011) Population genetics of genomics-based crop improvement methods. Trends in Genetics 27, 98–106.
Population genetics of genomics-based crop improvement methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsV2htro%3D&md5=c9925aef5b32994d8feda9bcfb2f9113CAS |

Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155, 2011–2014.

Hudson RR (2002) Generating samples under a Wright–Fisher neutral model of genetic variation. Bioinformatics 18, 337–338.
Generating samples under a Wright–Fisher neutral model of genetic variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFentrw%3D&md5=fbec188edf66396b811481f03aa6898bCAS |

Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589.

Hyten DL, Choi IY, Song QJ, Shoemaker RC, Nelson RL, Costa JM, Specht JE, Cregan PB (2007) Highly variable patterns of linkage disequilibrium in multiple soybean populations. Genetics 175, 1937–1944.
Highly variable patterns of linkage disequilibrium in multiple soybean populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFylsL4%3D&md5=ddd92a4913b5e6446a6c746dd7e78036CAS |

Ingvarsson P (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180, 329–340.
Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula.Crossref | GoogleScholarGoogle Scholar |

Kami J, Velásquez VB, Debouck DG, Gepts P (1995) Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proceedings of the National Academy of Sciences of the United States of America 92, 1101–1104.
Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslegs7w%3D&md5=5529c4e36d62304aba88a2fc2604b123CAS |

Kaplan L, Kaplan L (1988) Genetic resources of Phaseolus beans: their maintenance, domestication, evolution and utilisation. In ‘Current plant science and biotechnology in agriculture’. (Ed. P Gepts) pp. 125–142. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Kaplan L, Lynch TF (1999) Phaseolus (Fabaceae) in archaeology: AMS. Economic Botany 53, 261–272.
Phaseolus (Fabaceae) in archaeology: AMS.Crossref | GoogleScholarGoogle Scholar |

Kaplan L, Lynch TF, Smith CE (1973) Early cultivated beans (Phaseolus vulgaris) from an intermontane Peruvian valley. Science 179, 76–77.
Early cultivated beans (Phaseolus vulgaris) from an intermontane Peruvian valley.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czpslGktg%3D%3D&md5=f5b8d0e47592b8bad85e18bac01cafc2CAS |

Khairallah MM, Sears BB, Adams MW (1992) Mitochondrial restriction fragment length polymorphisms in wild Phaseolus vulgaris L.: insights on the domestication of the common bean. Theoretical and Applied Genetics 84, 915–922.
Mitochondrial restriction fragment length polymorphisms in wild Phaseolus vulgaris L.: insights on the domestication of the common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnsVGntg%3D%3D&md5=d99ec7e6180ea21772c7604e3b54c94cCAS |

Kilian B, Ozkan H, Walther A, Kohl J, Dagan T, Salamini F, Martin W (2007) Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture. Molecular Biology and Evolution 24, 2657–2668.
Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVGjuw%3D%3D&md5=5ee0e68b68248e2a65e0cd3efc6ea229CAS |

Knowler WC, Williams RC, Pettitt DJ, Steinberg AG (1988) Gm3;5,13,14 and type 2 diabetes mellitus: an association in American Indians with genetic admixture. American Journal of Human Genetics 43, 520–526.

Koenig R, Gepts P (1989) Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of genetic diversity. Theoretical and Applied Genetics 78, 809–817.
Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of genetic diversity.Crossref | GoogleScholarGoogle Scholar |

Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common bean. Crop Science 36, 1037–1044.
Genetic control of the domestication syndrome in common bean.Crossref | GoogleScholarGoogle Scholar |

Kwak M, Gepts P (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theoretical and Applied Genetics 118, 979–992.
Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis12gsLo%3D&md5=79c951371d3080fa3cd3e0c9ac821874CAS |

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 Science 49, 554–563.
The putative Mesoamerican domestication center of Phaseolus vulgaris is located in the Lerma-Santiago basin of Mexico.Crossref | GoogleScholarGoogle Scholar |

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=e14681fe79aeb2676112db754dffc0f6CAS |

Leuenberger C, Wegmann D (2010) Bayesian computation and model selection without likelihoods. Genetics 184, 243–252.
Bayesian computation and model selection without likelihoods.Crossref | GoogleScholarGoogle Scholar |

Li X, Tan L, Zhu Z, Huang H, Liu Y, Hu S, Sun C (2009) Patterns of nucleotide diversity in wild and cultivated rice. Plant Systematics and Evolution 281, 97–106.
Patterns of nucleotide diversity in wild and cultivated rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXoslalu7c%3D&md5=f5684956bf848627c6f70aa2136cbd5cCAS |

Liu A, Burke JM (2006) Patterns of nucleotide diversity in wild and cultivated sunflower. Genetics 173, 321–330.
Patterns of nucleotide diversity in wild and cultivated sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvF2itrw%3D&md5=cc0e92d9cf2fe4a1ed6a6739a7b87015CAS |

Lopes JS, Beaumont ME (2010) ABC: a useful Bayesian tool for the analysis of population data. Infection, Genetics and Evolution 10, 825–832.
ABC: a useful Bayesian tool for the analysis of population data.Crossref | GoogleScholarGoogle Scholar |

Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111, 675–689.

McBryde F (1947) Cultural and historical geography of southwest Guatemala. Smithsonian Institute Publication 4, 1–184.

McClean PE, Lee RK (2007) Genetic architecture of chalcone isomerase non-coding regions in common bean (Phaseolus vulgaris L.). Genome 50, 203–214.
Genetic architecture of chalcone isomerase non-coding regions in common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlOguro%3D&md5=93bc4e1f82fb734cccf8dde332ffcf54CAS |

McClean P, Lee R, Miklas P (2004) Sequence diversity analysis of dihydroflavonol 4-reductase intron 1 in common bean. Genome 47, 266–280.
Sequence diversity analysis of dihydroflavonol 4-reductase intron 1 in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksFOrs7Y%3D&md5=a6a9b93593d7c6fef1ec7b5ccb290b71CAS |

McClean PE, Terpstra J, McConnell M, White C, Lee R, Mamidi S (2011) Population structure and genetic differentiation among the USDA common bean (Phaseolus vulgaris L.) core collection. Genetic Resources and Crop Evolution in press.

McConnell M, Mamidi S, Lee R, Chikara S, Rossi M, Papa R, McClean P (2010) Syntenic relationships among legumes revealed using a gene-based genetic linkage map of common bean (Phaseolus vulgaris L.) Theoretical and Applied Genetics 121, 1103–1116.
Syntenic relationships among legumes revealed using a gene-based genetic linkage map of common bean (Phaseolus vulgaris L.)Crossref | GoogleScholarGoogle Scholar |

Moeller DA, Tenaillon MI, Tiffin P (2007) Population structure and its effects on patterns of nucleotide polymorphism in teosinte (Zea mays ssp. parviglumis). Genetics 176, 1799–1809.
Population structure and its effects on patterns of nucleotide polymorphism in teosinte (Zea mays ssp. parviglumis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3P&md5=df432f8a512bc01b2ac4920d3bc2115bCAS |

Morrell PL, Toleno DM, Lundy KE, Clegg MT (2005) Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilisation. Proceedings of the National Academy of Sciences of the United States of America 102, 2442–2447.
Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFKitLk%3D&md5=91aec95315c37c5aa3f0affa4e4244efCAS |

Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell Online 21, 2194–2202.
Association mapping: critical considerations shift from genotyping to experimental design.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12qsL3P&md5=a3136696d920edf94476f6a5d5d2b662CAS |

Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloff JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nature Genetics 30, 190–193.
The extent of linkage disequilibrium in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFWltLo%3D&md5=db47699745f432c49bac458fa890720fCAS |

Otero-Arnaiz A, Casas A, Hamrick JL, Cruse-Sanders J (2005) Genetic variation and evolution of Polaskia chichipe (Cactaceae) under domestication in the Tehucan Valley, central Mexico. Molecular Ecology 14, 1603–1611.
Genetic variation and evolution of Polaskia chichipe (Cactaceae) under domestication in the Tehucan Valley, central Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVeqsbo%3D&md5=ae0abf7671d0a94ef79382d62b087749CAS |

Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theoretical and Applied Genetics 106, 239–250.

Papa R, Acosta J, Delgado-Salinas A, Gepts P (2005) A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica. Theoretical and Applied Genetics 111, 1147–1158.
A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2ksbjL&md5=1fb912c49048e7a0f2be2f6d9dac3c16CAS |

Papa R, Bellucci E, Rossi M, Leonardi S, Rau D, Gepts P, Nanni L, Attene G (2007) Tagging the signatures of domestication in common bean (Phaseolus vulgaris) by means of pooled DNA samples. Annals of Botany 100, 1039–1051.
Tagging the signatures of domestication in common bean (Phaseolus vulgaris) by means of pooled DNA samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVartg%3D%3D&md5=f8787d665e4ed2d40e67d4e2695f4b43CAS |

Pascual M, Chapuis MP, Mestres F, Balanyà J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of Drosophila subobscurain the New World: a microsatellite based survey using ABC methods. Molecular Ecology 16, 3069–3083.
Introduction history of Drosophila subobscurain the New World: a microsatellite based survey using ABC methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVertrfK&md5=93af63e959f5b968a439918e50563f84CAS |

Patin E, Laval G, Barreiro LB, Salas A, Semino O, Santachiara-Benerecetti S, Kidd KK, Kidd JR, Van der Veen L, Hombert JM, Gessain A, Froment A, Bahuchet S, Heyer E, Quintana-Murci L (2009) Inferring the demographic history of African farmers and pygmy hunter-gatherers using a multilocus resequencing data set. PLOS Genetics 5, e1000448
Inferring the demographic history of African farmers and pygmy hunter-gatherers using a multilocus resequencing data set.Crossref | GoogleScholarGoogle Scholar |

Piperno DR, Flannery KV (2001) The earliest archaeological maize (Zea mays L.) from highland Mexico: new accelerator mass spectrometry dates and their implications. Proceedings of the National Academy of Sciences of the United States of America 98, 2101–2103.
The earliest archaeological maize (Zea mays L.) from highland Mexico: new accelerator mass spectrometry dates and their implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVWitLk%3D&md5=40f000dce0795faa669a7bce89f1936bCAS |

Pozzi C, Rossini L, Vecchietti A, Salamini F (2004) Gene and genome changes during domestication. In ‘Cereal genomics’. (Eds PK Gupta, RK Varshney) pp. 165–198. (Kluwier Academic Publishers: London)

Pritchard JK, Seielstad MT, Perez-Lezaun A, Feldman MW (1999) Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Molecular Biology and Evolution 16, 1791–1798.

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

Pyhajarvi T, Garcia-Gil MR, Knurr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177, 1713–1724.
Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFSrtg%3D%3D&md5=985ea9810f980295bdc5848a51b9e0b7CAS |

Ray N, Wegmann D, Fagundes NJR, Wang S, Ruiz-Linares A, Excoffier L (2010) A statistical evaluation of models for the initial settlement of the American continent emphasizes the importance of gene flow with Asia. Molecular Biology and Evolution 27, 337–345.
A statistical evaluation of models for the initial settlement of the American continent emphasizes the importance of gene flow with Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntlGnug%3D%3D&md5=2d8afe08fd09d420bd4566c73f5bd7a9CAS |

Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proceedings of the National Academy of Sciences of the United States of America 98, 11479–11484.
Structure of linkage disequilibrium and phenotypic associations in the maize genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1yqu7s%3D&md5=a8fdda95b8c7e3327876d2dd5d6e93a2CAS |

Ross-Ibarra J, Morrell PL, Gaut BS (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proceedings of the National Academy of Sciences of the United States of America 104, 8641–8648.
Plant domestication, a unique opportunity to identify the genetic basis of adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFCqu7k%3D&md5=00ec0b81969e56e3ca9bc715dc255069CAS |

Rossi M, Bitocchi E, Bellucci E, Nanni L, Rau D, Attene G, Papa R (2009) Linkage disequilibrium and population structure in wild and domesticated populations of Phaseolus vulgaris L. Evolutionary Applications 2, 504–522.
Linkage disequilibrium and population structure in wild and domesticated populations of Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar |

Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF, Graner A, Close TJ, Waugh R (2006) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proceedings of the National Academy of Sciences of the United States of America 103, 18656–18661.
Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlahtrfP&md5=c7fac75f07a3a4ccbda3d1ccdeb6cf0aCAS |

Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.
DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisVOksrY%3D&md5=b05aa94b4a1cba8ac81ff8311e4d530aCAS |

Scheinfeldt LB, Biswas S, Madeoy J, Connelly CF, Schadt EE, Akey JM (2009) Population genomic analysis of ALMS1 in humans reveals a surprisingly complex evolutionary history. Molecular Biology and Evolution 26, 1357–1367.
Population genomic analysis of ALMS1 in humans reveals a surprisingly complex evolutionary history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSnt7k%3D&md5=11dfc6b45579c4fc0854206538f85e9bCAS |

Singh SP, Gepts P, Debouck DG (1991a) Races of common bean (Phaseolus vulgaris, Fabaceae). Economic Botany 45, 379–396.
Races of common bean (Phaseolus vulgaris, Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Singh SP, Nodari R, Gepts P (1991b) Genetic diversity in cultivated common bean: I. Allozymes. Crop Science 31, 19–23.
Genetic diversity in cultivated common bean: I. Allozymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhvVahsLo%3D&md5=a30eae4de75e68219b581fc282a68826CAS |

Smith B (1995) ‘The emergence of agriculture.’ (Scientific American Library: New York)

Sonnante G, Stockton T, Nodari RO, Becerra Velásquez VL, Gepts P (1994) Evolution of genetic diversity during the domestication of common-bean (Phaseolus vulgaris L.). Theoretical and Applied Genetics 89, 629–635.
Evolution of genetic diversity during the domestication of common-bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |

Staden R (1996) The Staden sequence analysis package. Molecular Biotechnology 5, 233–241.
The Staden sequence analysis package.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlt1Sgsb8%3D&md5=16557e841e64900c520389b437a4ddcaCAS |

Stewart CN, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Reviews. Genetics 4, 806–817.
Transgene introgression from genetically modified crops to their wild relatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1aksLc%3D&md5=ceffa605581b347139417da695dd3b9bCAS |

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.

Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277, 1063–1066.
Seed banks and molecular maps: unlocking genetic potential from the wild.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsFSisrw%3D&md5=f13f988337a844632fca565639492c2bCAS |

Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Molecular Biology and Evolution 21, 1214–1225.
Selection versus demography: a multilocus investigation of the domestication process in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlKlsrk%3D&md5=ec65c77df64b33221b07715a6cf98c95CAS |

Tohme J, Gonzalez D, Beebe S, Duque MC (1996) AFLP analysis of gene pools of a wild bean core collection. Crop Science 36, 1375–1384.
AFLP analysis of gene pools of a wild bean core collection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFCkurk%3D&md5=45135bab45050255eb5a1361cfc3998cCAS |

Vasemagi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Molecular Biology and Evolution 22, 1067–1076.
Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.).Crossref | GoogleScholarGoogle Scholar |

Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Molecular Biology and Evolution 22, 506–519.
Molecular population genetics and the search for adaptive evolution in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Krurs%3D&md5=a2e0db2739c2269f97e257183c685259CAS |

Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artificial selection on the maize genome. Science 308, 1310–1314.
The effects of artificial selection on the maize genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Ciur0%3D&md5=9ddead049a4f0c302c398552ec2dffb8CAS |

Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLOS Genetics 3, e4
An Arabidopsis example of association mapping in structured samples.Crossref | GoogleScholarGoogle Scholar |

Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB (2003) Single-nucleotide polymorphisms in soybean. Genetics 163, 1123–1134.

Zhu Q, Zheng X, Luo J, Gaut BS, Ge S (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Molecular Biology and Evolution 24, 875–888.
Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlersLo%3D&md5=dad43b88b3aa44d9e9824981e1743199CAS |