Genetic Resources and Crop Evolution

, Volume 64, Issue 5, pp 867–887 | Cite as

Genetic basis for folk classification of oca (Oxalis tuberosa Molina; Oxalidaceae): implications for research and conservation of clonally propagated crops

  • Lauren J. Moscoe
  • Raúl Blas
  • Daniel Huamán Masi
  • Modesto Huamán Masi
  • Eve Emshwiller
Research Article


Clonally propagated crops exhibit great diversity and are integral components of global and regional food systems. At the same time, little is known about the mechanisms that generate diversity within clonal crop species, and this diversity is increasingly threatened by economic, environmental, and social change. Research addressing the genetic basis for folk classification of clonal crops can address both of these challenges. Here, we carry out such research through a case study of the Andean tuber crop, oca (Oxalis tuberosa Molina). We employ ethnobotanical and molecular genetic methods to assess the congruence in partitioning of 216 oca accessions with respect to 26 folk taxa and with respect to 31 genetic clones. We find that the greatest number of folk taxa (11) correspond to single, unique genetic clones, but we also identify two instances of single folk taxa comprising multiple genetic clones and two instances of multiple folk taxa comprising single, shared genetic clones. We discuss the potential roles of different diversity-generating mechanisms, such as somaclonal variation and sexual reproduction, underlying these varied forms of congruence in order to inspire more directed research on this topic. We also discuss the implications of our findings on in situ and ex situ conservation work, in which practitioners often approximate crop genetic diversity by counting folk taxa. Ultimately, we argue that efforts to understand and conserve clonal crop diversity will be most effective when both folk classification and its genetic basis are considered together.


Agrobiodiversity Andean root and tuber crops Clonal crops In situ conservation Microsatellites Oxalis tuberosa Traditional ecological knowledge 


Los cultivos propagados por clones muestran una gran diversidad y son componentes integrales de los sistemas alimentarios globales y regionales. Al mismo tiempo, se sabe poco sobre los mecanismos que generan la diversidad dentro de las especies de los cultivos clonales, y la amenaza a esta diversidad aumenta cada vez más por los cambios económicos, medioambientales y sociales. Ambos desafíos pueden abordarse con las investigaciones sobre la base genética de la clasificación campesina de los cultivos clonales. Por ello, se llevó a cabo esta investigación por medio de un estudio de caso del tubérculo andino, oca (Oxalis tuberosa Molina). Se empleó métodos etnobotánicos y genéticos moleculares para evaluar la congruencia de la clasificación de 216 entradas de oca con respeto a 26 taxones campesinos y a 31 clones genéticos. Se encontró que el número más alto de los taxones campesinos (11) corresponde a clones genéticos individuales y únicos, pero también se identificó dos casos en que los taxones campesinos individuales constan de múltiples clones genéticos y dos casos en que múltiples taxones campesinos constan de clones genéticos únicos y compartidos. Se discuten los roles potenciales de los distintos mecanismos de generación de la diversidad que subyacen estas formas variadas de la congruencia, como la variación somaclonal y la reproducción sexual, para incentivar más la investigación dirigida en este tema. También se discuten de las implicaciones de nuestros resultados en el los trabajos de conservación in situ y ex situ, en que es común aproximar la diversidad genética de cultivos por medio del conteo de los taxones campesinos. Por último, argumentamos que los esfuerzos por entender y conservar la diversidad de los cultivos clonales tendrán más éxito cuando se tome en cuenta la clasificación campesina junto con su base genética.

Palabras claves

Agrobiodiversidad Conocimiento ecológico tradicional Conservación in situ Cultivos clonales Microsatélites Oxalis tuberosa Raíces y tubérculos andinos 



Les agradecemos a los participantes de la comunidad de Viacha por su generosidad de tiempo y de conocimientos, con mención especial a la familia Maqque Ccoyo (Doña Berta, Don Visitación, Doña Vacilia, Analí, Sandra, y María Isabel). Les agradecemos también a los compañeros de Taray, especialmente a la familia Huamán Masi (Don Venancio, Doña Florencia, Roxana, e Hidalgo), por su gran ayuda en la chakra de oca. Además, gracias siempre a la familia Medina Noriega (Tulio, Consuelo, Masiel, Samira, Dina, y Lauren) por su apoyo y hospitalidad en Lima. Thank you to Marie Adams for technical advice regarding microsatellites; Jane Lee and Nikki Hare for laboratory assistance; Bret Larget for support with statistical analyses; Sarah Friedrich for assistance with figures; and members of the Emshwiller lab for encouragement at all stages of this research. We gratefully acknowledge our generous funding sources: University of Wisconsin-Madison Department of Botany (Judy Croxdale Award for Women in Science, Davis Research Grant, ON and EK Allen Fellowship), Latin American, Caribbean, and Iberian Studies Program (Nave Summer Field Research Grant), and Graduate School (Vilas Research Travel Grant); Sigma Delta Epsilon—Graduate Women in Science National Fellowship Program (Nell Mondy Fellowship) and Beta Chapter (Ruth Dickie Scholarship); and the Returned Peace Corps Volunteers of Wisconsin-Madison.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights statement

As described in Methods, we obtained written and/or oral permission to conduct research in Viacha from the community council and from each informant. Permissions were also obtained from Peru’s Instituto Nacional de Innovación Agraria (0284-2013-SUBDIRGEB-DIA/J and 0290-2013-SUBDIRGEB-DIA/J) and from the University of Wisconsin-Madison Education and Social/Behavioral Science Institutional Review Board (SE-2011-0201).

Supplementary material

10722_2016_407_MOESM1_ESM.pdf (329 kb)
Supplementary material 1 (PDF 328 kb)
10722_2016_407_MOESM2_ESM.pdf (266 kb)
Supplementary material 2 (PDF 266 kb)


  1. Academia Mayor de la Lengua Quechua (2005) Diccionario: Quechua-Español-Quechua, 2nd edn. Gobierno Regional Cusco, Cusco, PeruGoogle Scholar
  2. Alexander PJ, Rajanikanth G, Bacon CD, Bailey CD (2007) Recovery of plant DNA using a reciprocating saw and silica-based columns. Mol Ecol Notes 7:5–9. doi: 10.1111/j.1471-8286.2006.01549.x CrossRefGoogle Scholar
  3. Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139. doi: 10.1111/j.1365-294X.2007.03535.x CrossRefPubMedGoogle Scholar
  4. Babil PK, Yasuhara D, Sakaguchi K (2012) Recurring somaclonal variation as a factor of intra-specific diversity observed in Dioscorea alata L. Trop Agric Dev 56:71–79. doi: 10.11248/jsta.56.71 Google Scholar
  5. Barthel S, Crumley C, Svedin U (2013) Bio-cultural refugia—safeguarding diversity of practices for food security and biodiversity. Global Environ Chang 23:1142–1152. doi: 10.1016/j.gloenvcha.2013.05.001 CrossRefGoogle Scholar
  6. Bellon MR, Gotor E, Caracciolo F (2015a) Assessing the effectiveness of projects supporting on-farm conservation of native crops: evidence from the high Andes of South America. World Dev 70:162–176. doi: 10.1016/j.worlddev.2015.01.014 CrossRefGoogle Scholar
  7. Bellon MR, Gotor E, Caracciolo F (2015b) Conserving landraces and improving livelihoods: how to assess the success of on-farm conservation projects. Int J Agric Sustain 13:167–182. doi: 10.1080/14735903.2014.986363 CrossRefGoogle Scholar
  8. Berlin B, Breedlove DE, Raven PH (1973) General principles of classification and nomenclature in folk biology. Am Anthropol 75:214–242CrossRefGoogle Scholar
  9. Bizuayehu T (2008) On Sidama folk identification, naming, and classification of cultivated enset (Ensete ventricosum) cultivars. Genet Resour Crop Evol 55:1359–1370. doi: 10.1007/s10722-008-9334-x CrossRefGoogle Scholar
  10. Bonnave M, Bleeckx G, Rojas Beltrán J, Maughan P, Flamand MC, Terrazas F, Bertin P (2014) Farmers’ unconscious incorporation of sexually-produced genotypes into the germplasm of a vegetatively-propagated crop (Oxalis tuberosa Mol.). Genet Resour Crop Evol 61:721–740. doi: 10.1007/s10722-013-0068-z CrossRefGoogle Scholar
  11. Bonnave M, Bleeckx T, Terrazas F, Bertin P (2015) Effect of the management of seed flows and mode of propagation on the genetic diversity in an Andean farming system: the case of oca (Oxalis tuberosa Mol.). Agric Human Values. doi: 10.1007/s10460-015-9646-3
  12. Bonneuil C, Goffaux R, Bonnin I, Montalent P (2012) A new integrative indicator to assess crop genetic diversity. Ecol Indic 23:280–289. doi: 10.1016/j.ecolind.2012.04.002 CrossRefGoogle Scholar
  13. Borgatti SP (1996) ANTHROPAC 4.0 methods guide. Analytic Technologies, Natick, MAGoogle Scholar
  14. Boster JS (1985) Selection for perceptual distinctiveness: evidence from Aguaruna cultivars of Manihot esculenta. Econ Bot 39:310–325. doi: 10.1007/BF02858802 CrossRefGoogle Scholar
  15. Bradbury EJ (2014) Understanding toxic domesticates: biochemistry and population genetics of manioc (Manihot esculenta) and oca (Oxalis tuberosa). Dissertation, University of Wisconsin-MadisonGoogle Scholar
  16. Bradbury EJ, Emshwiller E (2011) The role of organic acids in the domestication of Oxalis tuberosa: a new model for studying domestication resulting in opposing crop phenotypes. Econ Bot 65:76–84. doi: 10.1007/s12231-010-9141-0 CrossRefGoogle Scholar
  17. Brush SB (1995) In situ conservation of landraces in centers of crop diversity. Crop Sci 35:346–354. doi: 10.2135/cropsci1995.0011183X003500020009x CrossRefGoogle Scholar
  18. Chang F, Qiu W, Zamar RH, Lazarus R, Wang X (2010) Clues: an R package for nonparametric clustering based on local shrinking. J Stat Softw. doi: 10.18637/jss.v033.i04 Google Scholar
  19. Cleveland DA, Soleri D (2007) Extending Darwin’s analogy: bridging differences in concepts of selection between farmers, biologists, and plant breeders. Econ Bot 61:121–136. doi:10.1663/0013-0001(2007)61[121:EDABDI]2.0.CO;2 CrossRefGoogle Scholar
  20. Cortes Bravo H (1976) Evaluación de mutaciones somáticas espontáneas en oca (Oxalis tuberosa Mol.). Centro de Investigación en Cultivos Andinos (CICA), Universidad Nacional San Antonio Abad del Cusco, Cusco, PeruGoogle Scholar
  21. Dansi A, Mignouna HD, Zoundjihekpon J, Sangare A, Asiedu R, Quin FM (1999) Morphological diversity, cultivar groups and possible descent in the cultivated yams (Dioscorea cayenensis/D. rotundata) complex in Benin Republic. Genet Resour Crop Evol 46:371–378. doi: 10.1023/A:1008698123887 CrossRefGoogle Scholar
  22. de Haan S, Bonierbale M, Ghislain M (2007) Indigenous biosystematics of Andean potatoes: folk taxonomy, descriptors and nomenclature. Presented at: 6th International Solanaceae Conference. Madison, WIGoogle Scholar
  23. Duputié A, 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 16:3025–3038. doi: 10.1111/j.1365-294X.2007.03340.x CrossRefPubMedGoogle Scholar
  24. Elias M, Panaud O, Robert T (2000a) Assessment of genetic variability in a traditional cassava (Manihot esculenta Crantz) farming system, using AFLP markers. Heredity 85:219–230. doi: 10.1046/j.1365-2540.2000.00749.x CrossRefPubMedGoogle Scholar
  25. Elias M, Rival L, McKey D (2000b) Perception and management of cassava (Manihot esculenta Crantz) diversity among Makushi Amerindians of Guyana (South America). J Ethnobiol 20:239–265Google Scholar
  26. Elias M, Penet L, Vindry P, McKey D, Panaud O, Robert T (2001) Unmanaged sexual reproduction and the dynamics of genetic diversity of a vegetatively propagated crop plant, cassava (Manihot esculenta Crantz), in a traditional farming system. Mol Ecol 10:1895–1907. doi: 10.1046/j.0962-1083.2001.01331.x CrossRefPubMedGoogle Scholar
  27. Emshwiller E (2002) Ploidy levels among species in the ‘Oxalis tuberosa alliance’ as inferred by flow cytometry. Ann Bot London 89:741–753. doi: 10.1093/aob/mcf135 CrossRefGoogle Scholar
  28. Emshwiller E (2006) Evolution and conservation of clonally propagated crops. In: Motley TJ, Zerega N, Cross HB (eds) Darwin’s harvest: new approaches to the origins, evolution, and conservation of crops. Columbia University Press, New York, pp 308–332Google Scholar
  29. Emshwiller E, Theim T, Grau A, Nina V, Terrazas F (2009) Origins of domestication and polyploidy in oca (Oxalis tuberosa; Oxalidaceae). 3. AFLP data of oca and four wild, tuber-bearing taxa. Am J Bot 96:1839–1848. doi: 10.3732/ajb.0800359 CrossRefPubMedGoogle Scholar
  30. Evans GC (1972) The quantitative analysis of plant growth. University of California Press, CaliforniaGoogle Scholar
  31. FAO (2010). The second report on the state of the world’s plant genetic resources for food and agriculture, Rome. Accessed 22 Oct 2015
  32. Galluzzi G, López Noriega I (2014) Conservation and use of genetic resources of underutilized crops in the Americas—a continental analysis. Sustainability 6:980–1017. doi: 10.3390/su6020980 CrossRefGoogle Scholar
  33. Gibson RW (2009) A review of perceptual distinctiveness in landraces including an analysis of how its roles have been overlooked in plant breeding for low-input farming systems. Econ Bot 63:242–255. doi: 10.1007/s12231-009-9086-3 CrossRefGoogle Scholar
  34. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19. doi: 10.18637/jss.v022.i07 CrossRefGoogle Scholar
  35. Guaraguara KJ (2013) Establecimiento de un kit de microsatelites en oca (Oxalis tuberosa Molina) para estudios de diversidad genética. M. Sc. Thesis, Universidad Mayor de San Simón, Cochabamba, BoliviaGoogle Scholar
  36. Hubert L, Arabie P (1985) Comparing partitions. J Classif 2:193–218. doi: 10.1007/BF01908075 CrossRefGoogle Scholar
  37. Jansky SH, Dawson J, Spooner DM (2015) How do we address the disconnect between genetic and morphological diversity in germplasm collections? Am J Bot 102:1213–1215. doi: 10.3732/ajb.1500203 CrossRefPubMedGoogle Scholar
  38. Jarvis DI, Brown AHD, Cuong PH, Collado-Panduro L, Latournerie-Moreno L, Gyawali S et al (2008) A global perspective of the richness and evenness of traditional crop-variety diversity maintained by farming communities. Proc Natl Acad Sci 105:5326–5331. doi: 10.1073/pnas.0800607105 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jarvis DI, Hodgkin T, Sthapit BR, Fadda C, Lopez-Noriega I (2011) An heuristic framework for identifying multiple ways of supporting the conservation and use of traditional crop varieties within the agricultural production system. CRC Crit Rev Plant Sci 30:125–176. doi: 10.1080/07352689.2011.554358 CrossRefGoogle Scholar
  40. Karamura D, Karamura E, Tushemereirwe W, Rubaihayo R (2010) Markham R (2010), Somatic mutations and their implications to the conservation strategies of the East African highland bananas (Musa spp.). Acta Hortic 879:615–621. doi: 10.17660/ActaHortic.879.68 CrossRefGoogle Scholar
  41. Kizito EB, Chiwona-Karltun L, Egwang T, Fregene M, Westerbergh A (2007) Genetic diversity and variety composition of cassava on small-scale farms in Uganda: an interdisciplinary study using genetic markers and farmer interviews. Genetica 130:301–318. doi: 10.1007/s10709-006-9107-4 CrossRefGoogle Scholar
  42. Lebot V, McKenna DJ, Johnston E, Zheng QY (1999) Morphological, phytochemical, and genetic variation in Hawaiian cultivars of’Awa (kava, Piper methysticum, Piperaceae). Econ Bot 53:407–418. doi: 10.1007/BF02866720 CrossRefGoogle Scholar
  43. Malice M, Martin N, Pissard A, Rojas-Beltran JA, Gandarillas A, Bertin P, Baudoin J-P (2007) A preliminary study of the genetic diversity of Bolivian oca (Oxalis tuberosa Mol.) varieties maintained in situ and ex situ through the utilization of ISSR molecular markers. Genet Resour Crop Evol 54:685–690. doi: 10.1007/s10722-006-9180-7 CrossRefGoogle Scholar
  44. Malice M, Bizoux JP, Blas R, Baudoin JP (2010) Genetic diversity of Andean tuber crop species in the in situ microcenter of Huanuco, Peru. Crop Sci 50:1915–1923. doi: 10.2135/cropsci2009.09.0476 CrossRefGoogle Scholar
  45. McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186:318–332. doi: 10.1111/j.1469-8137.2010.03210.x CrossRefPubMedGoogle Scholar
  46. Moscoe LJ, Emshwiller E (2015) Diversity of Oxalis tuberosa Molina: a comparison between AFLP and microsatellite markers. Genet Resour Crop Evol 62:335–347. doi: 10.1007/s10722-014-0154-x CrossRefGoogle Scholar
  47. Moscoe LJ, Emshwiller E (2016) Farmer perspectives on oca (Oxalis tuberosa Molina; Oxalidaceae) diversity conservation: values and threats. J Ethnobiol, in pressGoogle Scholar
  48. Noyer JL, Causse S, Tomekpe K, Bouet A, Baurens FC (2005) A new image of plantain diversity assessed by SSR, AFLP and MSAP markers. Genetica 124:61–69. doi: 10.1007/s10709-004-7319-z CrossRefPubMedGoogle Scholar
  49. Peroni N, Kageyama PY, Begossi A (2007) Molecular differentiation, diversity, and folk classification of “sweet” and “bitter” cassava (Manihot esculenta) in Caiçara and Caboclo management systems (Brazil). Genet Resour Crop Evol 54:1333–1349. doi: 10.1007/s10722-006-9116-2 CrossRefGoogle Scholar
  50. Pissard A, Rojas Beltran JA, Faux AM, Paulet S, Bertin P (2008) Evidence of intra-varietal genetic variability in the vegetatively propagated crop oca (Oxalis tuberosa Mol.) in the Andean traditional farming system. Plant Syst Evol 270:59–74. doi: 10.1007/s00606-007-0605-3 CrossRefGoogle Scholar
  51. Pujol B, Renoux F, Elias M, Rival L, McKey D (2007) The unappreciated ecology of landrace populations: conservation consequences of soil seed banks in cassava. Biol Cons 136:541–551. doi: 10.1016/j.biocon.2006.12.025 CrossRefGoogle Scholar
  52. R Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. Accessed 1 Feb 2012
  53. Sadiki M, Jarvis DI, Rijal D, Bajracharya J, Hue NN, Camacho-Villa TC, Burgos-May LA et al (2010) Variety names: an entry point to crop genetic diversity and distribution in agroecosystems? In: Jarvis DI, Padoch D, Cooper HD (eds) Managing biodiversity in agricultural ecosystems. Bioversity international, New York, pp 34–76Google Scholar
  54. Scott KD, Ablett EM, Lee LS, Henry RJ (2000) AFLP markers distinguishing an early mutant of Flame Seedless grape. Euphytica 113:243–247. doi: 10.1023/A:1003977408214 CrossRefGoogle Scholar
  55. Scurrah M, Celis-Gamboa C, Chumbiauca S, Salas A, Visser RGF (2008) Hybridization between wild and cultivated potato species in the Peruvian Andes and biosafety implications for deployment of GM potatoes. Euphytica 164:881–892. doi: 10.1007/s10681-007-9641-x CrossRefGoogle Scholar
  56. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285. doi: 10.1038/nrg2072 CrossRefPubMedGoogle Scholar
  57. Soleri D, Worthington M, Aragón-Cuevas F, Smith SE, Gepts P (2013) Farmers’ varietal identification in a reference sample of local Phaseolus species in the Sierra Juárez, Oaxaca, Mexico. Econ Bot 67:283–298. doi: 10.1007/s12231-013-9248-1 CrossRefGoogle Scholar
  58. Sorensen T (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Biol Skrif 5:1–34Google Scholar
  59. Steinley D (2004) Properties of the Hubert-Arabie adjusted Rand index. Psychol Methods 93:386–396. doi: 10.1037/1082-989X.9.3.386 CrossRefGoogle Scholar
  60. Terrazas F, Valdivia G (1998) Spatial dynamics of in situ conservation: handling the genetic diversity of Andean tubers in mosaic systems Pl. Genet Res Newsl 114:9–15Google Scholar
  61. Tesfaye B, Lüdders P (2003) Diversity and distribution patterns of enset landraces in Sidama, Southern Ethiopia. Genet Resour Crop Evol 50:359–371. doi: 10.1023/A:1023918919227 CrossRefGoogle Scholar
  62. Trognitz BR, Hermann M, Carrión S (1998) Germplasm conservation of oca (Oxalis tuberosa Mol.) through botanical seed. Seed formation under a system of polymorphic incompatibility. Euphytica 101:133–141. doi: 10.1023/A:1018336003573 CrossRefGoogle Scholar
  63. Turumaya AA (2011) Desarrollo de marcadores microsatélites para la caracterización de germoplasma en oca (Oxalis tuberosa Molina). M. Sc. Thesis, Universidad Mayor de San Simón, Cochabamba, BoliviaGoogle Scholar
  64. Vandenbroucke H, Mournet P, Vignes H, Chaïr H, Malapa R, Duval MF, Lebot V (2016) Somaclonal variants of taro (Colocasia esculenta Schott) and yam (Dioscorea alata L.) are incorporated into farmers’ varietal portfolios in Vanuatu. Genet Resour Crop Evol 63:495–511. doi: 10.1007/s10722-015-0267-x CrossRefGoogle Scholar
  65. Wright SD, McConnaughay KDM (2002) Interpreting phenotypic plasticity: the importance of ontogeny. Plant Spec Biol 17:119–131. doi: 10.1046/j.1441 CrossRefGoogle Scholar
  66. Xu J, Yang Y, Pu Y, Ayad WG, Eyzaguirre PB (2001) Genetic diversity in taro (Colocasia esculenta Schott, Araceae) in China: an ethnobotanical and genetic approach. Econ Bot 55:14–31. doi: 10.1007/BF02864543 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Lauren J. Moscoe
    • 1
  • Raúl Blas
    • 2
  • Daniel Huamán Masi
    • 2
  • Modesto Huamán Masi
    • 3
  • Eve Emshwiller
    • 1
  1. 1.Department of BotanyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Facultad de AgronomíaUniversidad Nacional Agraria La MolinaLimaPeru
  3. 3.Facultad de Agronomía y ZootecniaUniversidad Nacional de San Antonio Abad del CuscoCuscoPeru

Personalised recommendations