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Conservation Genetics

, Volume 15, Issue 6, pp 1315–1328 | Cite as

Wild to crop introgression and genetic diversity in Lima bean (Phaseolus lunatus L.) in traditional Mayan milpas from Mexico

  • Dzul-Tejero Félix
  • Julián Coello-Coello
  • Jaime Martínez-CastilloEmail author
Research Article

Abstract

Despite the evolutionary, ecological and economic importance of introgression between a domesticated species and its wild relatives in centers of diversity and domestication, the role of traditional farmers in this process has received limited attention. In the Yucatan Peninsula, the region of Mexico that has the greatest amount of domesticated varieties of Lima bean, wild populations grow sympatrically with conspecific varieties, allowing the Mayan farmer to act directly on introgressed seed. We used 11 microsatellite loci to assess levels of introgression in three wild-domesticated complexes of Lima bean from the Yucatan Peninsula and analyze its impact on the genetic diversity of this crop. structure and InStruct analyses showed similar results. The Instruct analysis indicated that the complex with the lowest level of introgression was one where the farmer actively selected against wild plants and introgressed seed. In contrast, the complex with the highest level of introgression was one where the farmer has been consciously selecting a weedy morphotype for 15 years and has already incorporated it into his diet. Genetic diversity of the domesticated pool was higher in the complex with the higher level of introgression. This study showed that farmers have an important role in limiting or favoring the wild to crop introgression and influencing the levels of genetic diversity in their domesticated pool. Only when traditional farmers’ knowledge is taken into account can we correctly understand the dynamics, generation and maintenance of genetic diversity of the landraces in the centers of diversity and domestication.

Keywords

Agricultural practices Gene flow Microsatellite markers Traditional Mayan farmers Seed selection Wild-domesticated complexes 

Notes

Acknowledgments

This paper is part of the research for the first author’s Master’s thesis at the Centro de Investigación Científica de Yucatán, A. C., postgraduate studies in Biological Sciences Option Natural Resources, conducted under the direction of Jaime Martínez-Castillo. We thank Patricia Colunga-GarcíaMarín, Daniel Zizumbo-Villarreal and Silvia Terán-Contreras for academic advice, and two anonymous reviewers for comments that improved the manuscript. The first author thanks the Consejo Nacional de Ciencia y Tecnología-Mexico for a scholarship for his postgraduate studies and Ciencia Básica-CONACYT (project number 54788) for financial support for the research. The authors thank B. Hazen for help reviewing the English.

References

  1. Altieri MA, Montecinos C (1993) Conserving crop genetic resources in Latin America through farmer’s participation. In: Christopher S, Potter DJ, Cohen JI (eds) Perspectives on biodiversity: case studies of genetic resource conservation and development. American Association for the Advancement of Science, Washinton, pp 45–64Google Scholar
  2. Anderson E (1949) Introgressive hybridization. Wiley, New YorkGoogle Scholar
  3. Andueza-Noh RH, Serrano-Serrano ML, Chacón Sánchez MI, Sánchez del Pino I, Camacho-Pérez L, Coello-Coello J, Mijangos Cortés J, Debouck DG, Martínez-Castillo J (2013) Multiple domestications of the Mesoamerican gene pool of Lima bean (Phaseolus lunatus L.): evidence from chloroplast DNA sequences. Genet Resour Crop Evol 60:1069–1086CrossRefGoogle Scholar
  4. Arnold ML (1992) Natural hybridization as an evolutionary process. Ann Rev Ecol Syst 23:237–261CrossRefGoogle Scholar
  5. Ballesteros GA (1999) Contribuciones al conocimiento del frijol Lima (Phaseolus lunatus L.) en América Tropical. PhD Thesis, Colegio de Posgraduados. Montecillos, Estado de MéxicoGoogle Scholar
  6. Bañuelos-Jimenes JS, Craig R, Lynch JP (2002) Salinity tolerance of species during germination and early seedling growth. Crop Sci 42:1584–1594CrossRefGoogle Scholar
  7. Barnaud A, Deu M, Garine E, Chantereau J, Bolteu J, Koïda EO, McKey D, Joly HI (2009) A weed–crop complex in sorghum: the dynamics of genetic diversity in a traditional farming system. Am J Bot 96(10):1869–1879PubMedCrossRefGoogle Scholar
  8. Barrantes D, Macaya G, Guarino L, Baudoin JP, Rocha OJ (2008) The impact of local extinction on genetic structure of wild populations of Lima beans (Phaseolus lunatus) in the Central Valley of Costa Rica: consequences for the conservation of plant genetic resources. Rev Biol Trop 56(3):1023–1041PubMedGoogle Scholar
  9. Baudet JC (1977) The taxonomic status of the cultivated types of Lima bean (Phaseolus lunatus L.). Trop Grain Legume Bull 7:29–30Google Scholar
  10. Baudoin JP, Degreef J, Hardy O, Janart F, Zoro Bi I (1998) Development of an in situ conservation strategy for wild Lima bean (Phaseolus lunatus L.) populations in the central valley of Costa Rica. In: Owens SJ, Rudall PJ (eds) Reproduction biology. Royal Botanic Garden Press, Kew, pp 417–426Google Scholar
  11. Beebe S, Toro O, Viviana G, Chacón MI, Debouck DG (1997) Wild-weed-crop complexes of common bean (Phaseolus vulgaris L., Fabaceae) in the Andes of Peru and Colombia, and their implications for conservation and breeding. Genet Resour Crop Evol 44:73–91CrossRefGoogle Scholar
  12. Bitterlich I, Upadhyaya MK, Shibairo SI (1996) Weed control in cole and onion (Allium cepa) crops using ammonium nitrate. Weed Sci Soc Am 44:952–958Google Scholar
  13. Brush SB (1995) In-situ conservation of landraces in centers of crop diversity. Crop Sci 35:346–354CrossRefGoogle Scholar
  14. Chandler S, Dunwell JM (2008) Gene flow, risk assessment and the environmental release of transgenic plants. Crit Rev Plant Sci 27(1):25–49CrossRefGoogle Scholar
  15. Chimal-Chan AM (2008) Polinización y flujo génico de Phaseolus lunatus L. en el sur de la Península de Yucatán. Bachelor Dissertation. Instituto Tecnológico de Conkal. Conkal, Yucatán, MéxicoGoogle Scholar
  16. CIRAD (2002) Coconut Microsatellite kit (A loboratory Manual), Training session. Montpellier, FranceGoogle Scholar
  17. Cortés AJ, Monserrate FA, Ramírez-Villegas J, Madriñán S, Blair MW (2013) Drought tolerance in wild plant populations: the case of common bean (Phaseolus vulgaris L.). PLoS ONE 8(5):e62898. doi: 10.1371/journal.pone.0062898 PubMedCentralPubMedCrossRefGoogle Scholar
  18. Coulibaly S, Pasquet RS, Papa R, Gepts P (2002) AFLP analysis of the phenetic organization and genetic diversity of Vigna unguiculata L. Walp. Reveals extensive gene flow between wild and domesticated types. Theor Appl Genet 104:358–366PubMedCrossRefGoogle Scholar
  19. Couturon E, Mariac C, Bezançon G, Lauga L, Renno JF (2003) Impact of natural and human selection on the frequency of the F1 hybrid between cultivated and wild pearl millet (Pennisetum glaucum (L.) R. Br.). Euphytica 133:329–337CrossRefGoogle Scholar
  20. Cuanalo de la C. HE, Arias-Reyes LM (1997) Cultural and economic factors that affect farmers decision-making in Yucatan, Mexico. Pág. 14 In: DI Jarvis, T Hodgkin (ed), Strengthening the scientific basis of in situ conservation of agricultural biodiversity on-farm. Options for data collecting and analysis. Workshop 25–29 Aug. 1997. IPGRI, Rome, ItalyGoogle Scholar
  21. Degreef J (1998) De´veloppement d’un mode `le de ´mographicque et applications a ` la conservation in situ de populations sauvages de haricot de Lima (Paseoulus lunatus L.) dans la valle ´e centrale du Costa Rica. PhD Thesis, Fac Univ Sci Agron. Gembloux, BelgiumGoogle Scholar
  22. Desplanque B, Boudry P, Broomberg K, Saumitou-Laprade P, Cuguen J, Van Dijk H (1999) Genetic diversity and gene flow between wild, cultivated and weedy forms of Beta vulgaris L. (Chenopodiaceae), assessed by RFLP and microsatellite markers. Theor Appl Genet 98:1194–1201CrossRefGoogle Scholar
  23. Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  24. Duputié A, David P, Debain C, McKey D (2007) Natural hybridization between a clonally propagated crop, cassava (Manihot esculenta Crantz) and a wild relative in French Guiana. Mol Ecol 16:3025–3038PubMedCrossRefGoogle Scholar
  25. Ejeta G, Grenier C (2005) Sorghum and its weedy hybrids. In: Gressel J (ed) Crop ferality and volunteerism. Taylor and Francis, Boca Raton, pp 123–135Google Scholar
  26. Elias M, McKey D, Panaud O, Anstett MC, Robert T (2001) Traditional management of cassava morphological and genetic diversity by the Makushi Amerindians (Guyana, South America): perspectives for on-farm conservation of crop genetic resources. Euphytica 120:143–157CrossRefGoogle Scholar
  27. Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Ann Rev Ecol Syst 30:539–563CrossRefGoogle Scholar
  28. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  29. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distance among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  30. Gaitán-Solís E, Duque MC, Edwards KJ, Tohme J (2002) Microsatellite repeats in common bean (Phaseolus vulgaris): isolation, characterization, and cross-species amplification in Phaseolus ssp. Crop Sci 42:2128–2136CrossRefGoogle Scholar
  31. Gao H, Williamson S, Bustamante CD (2007) An MCMC approach for joint inference of population structure and inbreeding rates from multi-locus genotype data. Genetics 176:1635–1651PubMedCentralPubMedCrossRefGoogle Scholar
  32. Gepts P, Papa R (2003) Possible effects of (trans)gene flow from crops on the genetic diversity from landraces and wild relatives. Environ Biosaf Res 2:89–103CrossRefGoogle Scholar
  33. Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New YorkGoogle Scholar
  34. Gray AJ (2005) Hybridization between crops and wild plants in the age of genetic engineering: new risks or new paradigms? Am J Bot 92(4):768–771CrossRefGoogle Scholar
  35. Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156:1–13CrossRefGoogle Scholar
  36. Harlan JR (1965) The possible role of weedy races in the evolution of cultivated plants. Euphytica 14:173–176CrossRefGoogle Scholar
  37. Hernández-Xolocotzi E (1959) La agricultura. In: Beltrán E (ed) Los recursos naturales del sureste y su aprovechamiento, vol 3. Instituto Mexicano de Recursos Naturales Renovables, México, pp 1–38Google Scholar
  38. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  39. Jarvis D (1999) Strengthening the scientific basis of in situ conservation of agricultural biodiversity on farm. Bot Lithuania 2(Suppl):79–90Google Scholar
  40. Jarvis DI, Hodgkin T (1999) Wild relatives and crop cultivars: detecting natural introgression and farmer selection of new genetic combinations in agroecosystems. Mol Ecol 8:159–173CrossRefGoogle Scholar
  41. Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  42. Lakis G, Ousmane A, Sanoussi D, Habibou A, Badamassi M, Lamy F, Jika N, Sidikou R, Adam T, Sarr A, Luxereau A, Robert T (2011) Evolutionary dynamics of cycle length in pear millet: the role of farmer’s practices and gene flow. Genetica 139:1367–1380PubMedCrossRefGoogle Scholar
  43. Mariac C, Robert T, Allinne C, Remigereau MS, Luxereau A, Tidjani M, SeyniO Bezancon G, Pham JL, Sarr A (2006) Genetic diversity and gene flow among pearl millet crop/weed complex: a case study. Theor Appl Genet 113:1003–1014PubMedCrossRefGoogle Scholar
  44. Martínez-Castillo J, Zizumbo-Villarreal D, Perales-Rivera H, Colunga-GarcíaMarín P (2004) Intraspecific diversity and morpho-phenological variation in Phaseolus lunatus L. from the Yucatan Peninsula, México. Econ Bot 58(3):354–380CrossRefGoogle Scholar
  45. Martínez-Castillo J, Zizumbo-Villarreal D, Gepts P, Delgado-Valerio P, Colunga-GarcíaMarín P (2006) Structure and genetic diversity of wild populations of lima BEAN (Phaseolus lunatus L.) from the Yucatan Peninsula, Mexico. Crop Sci 46:1071–1080CrossRefGoogle Scholar
  46. Martínez-Castillo J, Zizumbo-Villarreal D, Gepts P, Colunga-GarcíaMarín P (2007) Gene flow and genetic structure in the wild-weedy-domesticated complex of Lima bean (P. lunatus L.) in its Mesoamerican center of domestication and diversity. Crop Sci 47:58–66CrossRefGoogle Scholar
  47. Martínez-Castillo J, Colunga-GarcíaMarín P, Zizumbo-Villarreal D (2008) Genetic erosion and in situ conservation of Lima bean (Phaseolus lunatus L.) landraces in its Mesoamerican diversity center. Genet Resour Crop Evol 55:1065–1077CrossRefGoogle Scholar
  48. Martínez-Castillo J, Camacho-Pérez L, Coello-Coello J, Andueza-Noh R (2011) Wholesale replacement of Lima bean (Phaseolus lunatus L.) landraces over the last 30 years in northeastern Campeche, Mexico. Genet Resour Crop Evol 59:191–204CrossRefGoogle Scholar
  49. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler I, Doebley JF (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084PubMedCentralPubMedCrossRefGoogle Scholar
  50. Motta-Aldana J, Serrano-Serrano ML, Torres HJ, Villamizar CG, Debouck DG, Chacón MI (2010) Multiple origins of lima bean landraces in the Americas: evidence from chloroplast and nuclear DNA polymorphisms. Crop Sci 50:1773–1787CrossRefGoogle Scholar
  51. Olsen K, Schaal B (2007) Insights on the evolution of a vegetatively propagated crop species. Mol Ecol 16:2838–2840PubMedCrossRefGoogle Scholar
  52. Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity on wild and domesticated common bean (Phaseolus lunatus L.) from Mesoamerica. Theor Appl Genet 106:239–250PubMedGoogle Scholar
  53. Papa R, Acosta J, Delgado-Salinas A, Gepts P (2005) A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica. Theor Appl Genet 111:1147–1158PubMedCrossRefGoogle Scholar
  54. Pérez-Toro A (1945) La agricultura milpera de los mayas de Yucatán. pp 173–204. In: LH Hoyos Villanueva, R Irigoyen-Rosado, R Ruz-Menéndez, H Lara-Lara (eds), Enciclopedia Yucatanense. Edición Oficial del Gobierno del Estado de Yucatán Vol. 6. MéxicoGoogle Scholar
  55. Pilson D, Prendeville RHR (2004) Ecological effects of transgenic crops and the escape of transgenes into wild populations. Annu Rev Ecol Evol Syst 35:149–174CrossRefGoogle Scholar
  56. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  57. Pujol B, David P, McKey D (2005) Microevolution in agri-cultural environments: how a traditional Amerindian farming practice favours heterozygosity in cassava (Manihot esculenta Crantz, Euphorbiaceae). Ecol Lett 8:138–147CrossRefGoogle Scholar
  58. Quiros CF, Ortega R, Van Raamsdonk LWD (1992) Amplification of potato genetic resources in their center of diversity: the role of natural outcrossing and selection by the Andean farmer. Genet Resour Crop Evol 39:107–113CrossRefGoogle Scholar
  59. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Evol Syst 27:83–109CrossRefGoogle Scholar
  60. Rosenberg NA (2002) Distruct: a program for the graphical display of structure results. http://www.cmb.usc.edu/»noahr/distruct. Accessed 1 Sept 2013Google Scholar
  61. Scarcelli N, Tostain S, Vigouroux Y (2006) Farmers’ use of wild relative and sexual reproduction in a vegetatively propagated crop. The case of yam in Benin. Mol Ecol 15:2421–2431PubMedCrossRefGoogle Scholar
  62. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  63. Serrano-Serrano ML, Hernández-Torres J, Castillo-Villamizar G, Debouck DG, Chacón MI (2010) Gene pools in wild Lima bean (Phaseolus lunatus L.) from the Americas: evidences for an Andean origin and past migrations. Mol Phylogenet Evol 54:76–87PubMedCrossRefGoogle Scholar
  64. Serrano-Serrano ML, Andueza-Noh RH, Martínez-Castillo J, Debouck DG, Chacón MI (2012) Evolution and domestication of Lima bean (Phaseolus lunatus L.) in Mexico: evidence from ribosomal DNA. Crop Sci 52:1698–1712CrossRefGoogle Scholar
  65. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792PubMedCrossRefGoogle Scholar
  66. StatPoint, Inc. (2006) Statgraphics Centurión XV. Version 15.2.05 1982–2007Google Scholar
  67. Suárez-Barón H, Martínez-Garay C, Gonzalez-Torres RI, Duque MC, Debouck DG, Thome J (2007) Determination of gene flow events in natural “wild-weedy-cultivated complexes in gene pools of Phaseolus lunatus L. External Program and Management Reviews (EPMRs). CIAT ColombiaGoogle Scholar
  68. Tautz D (1989) Hypervariability of simple secuence as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471PubMedCentralPubMedCrossRefGoogle Scholar
  69. Teshome A, Baum BR, Fahrig L, Torrance JK, Arnasen TJ, Lambert JH (1997) Sorghum (Sorghum bicolor L.) landrace variation and classification in north Shewa and South Welo, Ethiopia. Euphytica 97:255–263CrossRefGoogle Scholar
  70. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  71. Van Raamsdonk LWD, Van Der Maesen LJG (1996) Crop-weed-complexes: the complex relationship between crop plants and their wild relatives. Acta Botánica Neerlandica 45:135–155CrossRefGoogle Scholar
  72. Viard F, Bernard J, Desplanque B (2002) Crop–weed interactions in the Beta vulgaris complex at a local scale: allelic diversity and gene flow within sugar beet fields. Theo App Genet 104:688–697CrossRefGoogle Scholar
  73. 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. PNAS 99:9650–9655PubMedCentralPubMedCrossRefGoogle Scholar
  74. Vijayan P, Parkin IA, Karcz SR, McGowan K, Vijayan K, Vandenberg A, Bett KE (2011) Captured cold-stress-related sequences diversity from a wild relative of common bean (Phaseolus angustissimus). Genome 54:620–628PubMedCrossRefGoogle Scholar
  75. Webster BD, Lynch SP, Tucker CL (1979) A morphological study of the development of reproductive structures of Phaseolus lunatus L. J Am Soc Hortic Sci 104:240–243Google Scholar
  76. Xu DH, Abe J, Gai JY, Shimamoto Y (2002) Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated cultivated soybeans. Theor Appl Genet 105:645–653PubMedCrossRefGoogle Scholar
  77. Yeh FC, Boyle TJB (1999). Popgene version 1.31. Microsoft window-based freeware for population analysis. University of Alberta and Centre for International Forestry Research, Edmonton, AlbertaGoogle Scholar
  78. Zizumbo-Villarreal D, Colunga-GarcíaMarín P, Payro E, Delgado-Valerio P, Gepts P (2005) Population structure and evolution dynamics of wild-weedy-domesticated complexes of common bean in a Mesoamerican region. Crop Sci 45:1073–1083CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Dzul-Tejero Félix
    • 1
  • Julián Coello-Coello
    • 1
  • Jaime Martínez-Castillo
    • 1
    Email author
  1. 1.Centro de Investigación Científica de Yucatán (CICY)MéridaMexico

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