Theoretical and Applied Genetics

, Volume 111, Issue 6, pp 1147–1158 | Cite as

A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica

Original Paper


Lack of introgression or divergent selection may be responsible for the maintenance of phenotypic differences between sympatric populations of crops and their wild progenitors. To distinguish between these hypotheses, amplified fragment length polymorphism markers were located on a molecular linkage map of Phaseolus vulgaris relative to genes for the domestication syndrome and other traits. Diversity for these same markers was then analyzed in two samples of wild and domesticated populations from Mesoamerica. Differentiation between wild and domesticated populations was significantly higher in parapatric and allopatric populations compared to sympatric populations. It was also significantly higher near genes for domestication compared to those away from these genes. Concurrently, the differences in genetic diversity between wild and domesticated populations were strongest around such genes. These data suggest that selection in the presence of introgression appears to be a major evolutionary factor maintaining the identity of wild and domesticated populations in sympatric situations. Furthermore, alleles from domesticated populations appear to have displaced alleles in sympatric wild populations, thus leading to a reduction in genetic diversity in such populations. These results also provide a possible experimental framework for assessing the long-term risk of transgene escape and the targeting of transgenes inside the genome to minimize the survival of these transgenes into wild populations following introduction by gene flow.


Gene Flow Wild Population Common Bean AFLP Marker Phaseolin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the McKnight Foundation. RP was supported by CNR (Italy) for his stay in Davis and work at Ancona. We thank Guido Barbujani, Thomas Bataillon, Isabelle Olivieri, Cal Qualset, Delphine Sicard, Julianno Sambatti, Don Strong, Fabio Veronesi and Renaud Vitalis for their useful comments on an early version of the manuscript.


  1. Burke JM, Tang S, Knapp SJ, Rieseberg LH (2002) Genetic analysis of sunflower domestication. Genetics 161:1257–1267PubMedGoogle Scholar
  2. Cavalli-Sforza LL (1966) Population structure and human evolution. Proc R Soc Lond Ser B 164:362–379ADSGoogle Scholar
  3. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibirum patterns of genetic diversity in subdivided populations. Genet Res 70:155–174CrossRefPubMedGoogle Scholar
  4. Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295PubMedGoogle Scholar
  5. Doebley J, Stec A, Wendel J, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population:implications for the origin of maize. Proc Natl Acad Sci USA 87:9888–9892PubMedADSGoogle Scholar
  6. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  7. Freyre R, Skroch P, Geffroy V, Adam-Blondon A-F, Shirmohamadali A, Johnson W, Llaca V, Nodari R, Pereira P, Tsai S-M, Tohme J, Dron M, Nienhuis J, Vallejos C, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core map and alignment of RFLP maps. Theor Appl Genet 97:847–856CrossRefGoogle Scholar
  8. Geffroy V, Sévignac M, De Oliveira J, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of QTL with genes involved in specific resistance. Mol Plant Microb Interact 13:287–296Google Scholar
  9. Gepts P (1988) Phaseolin as an evolutionary marker. In: Gepts P (ed) Genetic resources of Phaseolus beans. Kluwer, Dordrecht, pp 215–241Google Scholar
  10. Gepts P (1999) Development of an integrated genetic linkage map in common bean (Phaseolus vulgaris L.) and its use. In: Singh S (ed) Bean breeding for the 21st century Kluwer, Dordrecht, pp 53–91, 389–400Google Scholar
  11. Gepts P (2004) Domestication as a long-term selection experiment. Plant Breed Rev 24(Part 2):1–44Google Scholar
  12. 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. Econ Bot 40:451–468Google Scholar
  13. González A, Wong A, Delgado-Salinas A, Papa R, Gepts P (2005) Assessment of inter simple sequence repeat markers to differentiate sympatric wild and domesticated populations of common bean (Phaseolus vulgaris L.). Crop Sci 35:606–615CrossRefGoogle Scholar
  14. Gressel J (1999) Tandem constructs: preventing the rise of superweeds. Trends Biotech 17:361–366CrossRefGoogle Scholar
  15. Ibarra-Pérez F, Ehdaie B, Waines G (1997) Estimation of outcrossing rate in common bean. Crop Sci 37:60–65CrossRefGoogle Scholar
  16. Kaplan L, Lynch T (1999) Phaseolus (Fabaceae) in archaeology: AMS radiocarbon dates and their significance for pre-Columbian agriculture. Econ Bot 53:261–272Google Scholar
  17. Koenig R, Gepts P (1989) Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of diversity. Theor Appl Genet 78:809–817CrossRefGoogle Scholar
  18. Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common-bean. Crop Sci 36:1037–1045CrossRefGoogle Scholar
  19. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189CrossRefGoogle Scholar
  20. Lin J-Z, Morrell PL, Clegg MT (2002) The influence of linkage and inbreeding on patterns of nucleotide sequence diversity at duplicate alcohol dehydrogenase loci in wild barley (Hordeum vulgare ssp. spontaneum). Genetics 162:2007–2015PubMedGoogle Scholar
  21. Llaca V, Gepts P (1996) Pulsed field gel electrophoresis analysis of the phaseolin locus region in Phaseolus vulgaris. Genome 39:722–729CrossRefPubMedGoogle Scholar
  22. McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291CrossRefGoogle Scholar
  23. Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903CrossRefGoogle Scholar
  24. Miklas P, Johnson W, Delorme R, Gepts P (2001) QTL conditioning physiological resistance and avoidance to white mold in dry bean. Crop Sci 41:309–315CrossRefGoogle Scholar
  25. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, p 512Google Scholar
  26. Nei M, Li W-H (1979) Mathematical models for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273PubMedMATHADSGoogle Scholar
  27. Nodari RO, Tsai SM, Guzmán P, Gilbertson RL, Gepts P (1993) Towards an integrated linkage map of common bean. 3. Mapping genetic factors controlling host-bacteria interactions. Genetics 134:341–350PubMedGoogle Scholar
  28. Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193CrossRefPubMedGoogle Scholar
  29. 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. Theor Appl Genet 106:239–250PubMedGoogle Scholar
  30. Papa R, Gepts P (2004) Asymmetric gene flow and introgression between wild and domesticated populations. In: Den Nijs D, Bartsch D, Sweet J (ed) Introgression from genetically modified plants into wild relatives and its consequences. CABI, Oxon, pp 125–138Google Scholar
  31. Payró de la Cruz E, Gepts P, Colunga GarciaMarín P, Zizumbo Villareal D (2005) Spatial distribution of genetic diversity in wild populations of Phaseolus vulgaris L. from Guanajuato and Michoacán, México. Genet Res Crop Evol (in press)Google Scholar
  32. Poncet V, Lamy F, Enjalbert J, Joly H, Sarr A, Robert T (1998) Genetic analysis of the domestication syndrome in pearl millet (Pennisetum glaucum L, Poaceae): inheritance of the major characters. Heredity 81:648–658CrossRefGoogle Scholar
  33. Poncet V, Lamy F, Devos K, Gale M, Sarr A, Robert T (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theor Appl Genet 100:147–159CrossRefGoogle Scholar
  34. Poncet V, Martel E, Allouis S, Devos K, Lamy F, Sarr A, Robert T (2002) Comparative analysis of QTLs affecting domestication traits between two domesticated × wild pearl millet (Pennisetum glaucum L., Poaceae) crosses. Theor Appl Genet 104:965–975CrossRefPubMedGoogle Scholar
  35. Schlötterer C (2003) Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet 19:32–38CrossRefPubMedGoogle Scholar
  36. Singh SP, Nodari R, Gepts P (1991) Genetic diversity in cultivated common bean. I. Allozymes. Crop Sci 31:19–23CrossRefGoogle Scholar
  37. Sokal R, Rohlf F (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  38. 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.). Theor Appl Genet 89:629–635CrossRefGoogle Scholar
  39. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688CrossRefPubMedGoogle Scholar
  40. Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225CrossRefPubMedGoogle Scholar
  41. Vigouroux Y, McMullen M, Hittinger CT, Houchins K, Schulz L, Kresovich S, Matsuoka Y, Doebley J (2002) Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc Natl Acad Sci USA 99:9650–9655CrossRefPubMedADSGoogle Scholar
  42. Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedGoogle Scholar
  43. Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  44. Xiong L, Liu K, Dai X, Xu C, Zhang Q (1999) Identification of genetic factors controlling domestication-related traits of rice using an F2 population of a cross between Oryza sativa and O. rufipogon. Theor Appl Genet 98:243–251CrossRefGoogle Scholar
  45. Zizumbo-Villarreal D, Colunga-GarcíaMarín P, Payró de la Cruz E, Delgado-Valerio P, Gepts P (2005) Population structure and evolutionary dynamics of wild–weedy–domesticated complexes of common bean in a Mesoamerican region. Crop Sci 35 (in press)Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • R. Papa
    • 1
    • 2
  • J. Acosta
    • 3
  • A. Delgado-Salinas
    • 4
  • P. Gepts
    • 1
  1. 1.Department of Plant Sciences, Section of Crop and Ecosystem SciencesUniversity of CaliforniaDavisUSA
  2. 2.Dipartimento di Scienze degli Alimenti, Facoltà di AgrariaUniversitá Politecnica delle MarcheAnconaItaly
  3. 3.Instituto Nacional de Investigaciones Forestales y AgropecuariasCampo Experimental del BajíoCelayaMexico
  4. 4.Instituto de BiologíaUniversidad Nacional Autónoma de MéxicoMéxico D.F.Mexico

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