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Implications of farmers’ seed exchanges for on-farm conservation of quinoa, as revealed by its genetic diversity in Chile

Published online by Cambridge University Press:  24 February 2012

F. F. FUENTES*
Affiliation:
Departamento de Agricultura del Desierto y Biotecnología, Universidad Arturo Prat, Casilla 121, Iquique, Chile
D. BAZILE
Affiliation:
CIRAD (Centre de Coopération Internationale en Recherche Agronomique pour le Développement), UPR47, GREEN, Montpellier, France PUCV, Instituto de Geografía, Av. Brasil 2241, Valparaíso, Chile
A. BHARGAVA
Affiliation:
Amity Institute of Biotechnology, Amity University Lucknow Campus, Lucknow-226010, India
E. A. MARTÍNEZ
Affiliation:
Centro de Estudios Avanzados en Zonas Aridas (CEAZA), La Serena, Chile and PhD Program on Applied Biology and Ecology (Dr-BEA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile
*
*To whom all correspondence should be addressed. Email: francfue@unap.cl

Summary

Quinoa cultivation in Chile presents an ancient and active complex of geographic, climatic, social and cultural interactions that has determined its current biodiversity in the three main growing zones (north, central and south). Importantly, these interactions involve the participation of farmers, whose activities are at the base of seed exchange networks due to their knowledge and in situ conservation of genetic diversity. The present study reports how a better understanding of farmers’ seed exchanges and local production practices could impact the genetic structure and diversity of quinoa at national scale in Chile. Using field interviews and characterization of 20 microsatellite genetic markers in a multi-origin set of 34 quinoa accessions representative of Chile and the South American region, the phenetic analysis of germplasm was consistent with the current classification of quinoa ecotypes present in Chile and Andean zone. This allowed the identification of five populations, which were represented by quinoa of Salares (northern Chile), Coastal/Lowlands (central and southern Chile), Highlands (Peru, Bolivia and Argentina) and Inter-Andean Valleys (Ecuador and Colombia). The highly informative quality of the markers used revealed a wide genetic diversity among main growing areas in Chile, which correlated well with natural geographical–edaphic–climatic and social–linguistic context to the expansion of quinoa biodiversity. Additionally, in addition to ancient seed exchanges, this process is still governed by the diverse agricultural practices of Andean farmers. Genetic erosion is considered an imminent risk due to small-scale farming, where the influence of increased migration of people to urban systems and export-driven changes to the agro-ecosystems may further reduce the diversity of quinoa plants in cultivation.

Type
Crops and Soils Research Papers
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aleman, J. (2009). Caractérisation de la diversité des variétés et des modes de culture du Quinoa dans les communautés Mapuche du Sud du Chili. PhD thesis, University of Montpellier, France.Google Scholar
Aleman, J., Thomet, M., Bazile, D. & Pham, J. L. (2010). Central role of nodal farmers in seed exchanges for biodiversity dynamics: example of ‘curadoras’ for the quinoa conservation in Mapuche communities in South Chile. In Innovation and Sustainable Development in Agriculture and Food: ISDA 2010, Montpellier, France, 28 June–1 July 2010 (Eds Coudel, E., Devautour, H., Soulard, C. & Hubert, B.), pp. 114. Montpellier, France: ISDA. Available online at: http://hal.archives-ouvertes.fr/docs/00/53/09/50/PDF/Aleman_Central-role.pdf (verified 15 Dec 2011).Google Scholar
Anabalón Rodriguiez, L. & Thomet Isla, M. (2009). Comparative analysis of genetic and morphologic diversity among quinoa accessions (Chenopodium quinoa Willd.) of the South of Chile and highland accessions. Journal of Plant Breeding and Crop Science 1, 210216.Google Scholar
Angioi, S. A., Rau, D., Attene, G., Nanni, L., Bellucci, E., Logozzo, G., Negri, V., Zeuli, P. L. S. & Papa, R. (2010). Beans in Europe: origin and structure of the European landraces of Phaseolus vulgaris L. Theoretical and Applied Genetics 121, 829843.Google Scholar
Badstue, L. B. (2006). Smallholder seed practices: Maize seed management in the Central Valleys of Oaxaca, Mexico. PhD thesis, Wageningen University, The Netherlands.Google Scholar
Bazile, D. & Abrami, G. (2008). Des modèles pour analyser ensemble les dynamiques variétales du sorgho dans un village malien. Cahiers Agricultures 17, 203209.Google Scholar
Bazile, D., Carrié, C., Vidal, A. & Negrete, J. (2011). Modélisation des dynamiques spatiales liées à la culture du quinoa dans le Nord chilien. M@ppemonde 102, 114.Google Scholar
Bazile, D. & Negrete, J. (2009). Quínoa y biodiversidad: ¿Cuáles son los desafíos regionales? Revista Geográfica de Valparaíso 42, 1141.Google Scholar
Bazile, D., Olguín, P. A., Núñez, L. & Negrete, J. (2010 b). Diversidad genética de la variedad “Blanca” de quínoa de la región central de Chile. In Memoria Resúmenes del III Congreso Mundial de la Quinua, 16 al 19 de Marzo de 2010 (Ed. Copa, R.), p. 35 (abstract). Oruro-Potosí, Bolivia, Oruro: FCAV-Universidad Técnica de Oruro.Google Scholar
Bazile, D., Sánchez, M., Espinoza, P. & Delatorre, J. (2010 c). Manejo campesino de las variedades de quínoa del altiplano chileno. In Memoria Resúmenes del III Congreso Mundial de la Quinua, 16 al 19 de Marzo de 2010 (Ed. Copa, R.), p. 125 (abstract). Oruro-Potosí, Bolivia, Oruro: FCAV-Universidad Técnica de Oruro.Google Scholar
Bazile, D., Thomet, M., Aleman, J. & Pham, J. L. (2010 a). Impactos de las redes sociales sobre los flujos de semillas. Aplicación al caso de la biodiversidad de quínoa de las comunidades Mapuches (región de la Araucanía, sur de Chile). In Memoria Resúmenes del III Congreso Mundial de la Quinua, 16 al 19 de Marzo de 2010 (Ed. Copa, R.), p. 123 (abstract). Oruro-Potosí, Bolivia, Oruro: FCAV-Universidad Técnica de Oruro.Google Scholar
Bazile, D. & Weltzien, E. (2008). Agrobiodiversités. Cahiers Agricultures, Special Issue 17, 73256.Google Scholar
Bellucci, E., Nanni, L., Bitocchi, E., Rossi, M. & Papa, R. (2011). Genetic diversity and geographic differentiation in the alternative legume Tripodion tetraphyllum (L.) Fourr. in North African populations. Plant Biology 13, 381390.Google Scholar
Bertero, H. D. (2001). Effects of photoperiod, temperature and radiation on the rate of leaf appearance in quinoa (Chenopodium quinoa Willd.) under field conditions. Annals of Botany 87, 495502.Google Scholar
Bertero, H. D., King, R. W. & Hall, A. J. (1999). Modelling photoperiod and temperature responses of flowering in quinoa (Chenopodium quinoa Willd.). Field Crops Research 63, 1934.Google Scholar
Bhargava, A. & Fuentes, F. F. (2010). Mutational dynamics of microsatellites. Molecular Biotechnology 44, 250266.Google Scholar
Bhargava, A., Shukla, S. & Ohri, D. (2006). Chenopodium quinoa – an Indian perspective. Industrial Crops and Products 23, 7387.CrossRefGoogle Scholar
Bhargava, A., Shukla, S. & Ohri, D. (2007 a). Genetic variability and interrelationship among various morphological and quality traits in quinoa (Chenopodium quinoa Willd.). Field Crops Research 101, 104116.Google Scholar
Bhargava, A., Shukla, S., Rajan, S. & Ohri, D. (2007 b). Genetic diversity for morphological and quality traits in quinoa (Chenopodium quinoa Willd.) germplasm. Genetic Resources and Crop Evolution 54, 167173.Google Scholar
Brookfield, H., Padoch, C., Parsons, H. & Stocking, M. (2002). Cultivating Biodiversity: Understanding, Analysing and Using Agricultural Diversity. London: ITDG Publishing and United Nations University.Google Scholar
Casini, P. (2002). Possibilita di introdurre la quinoa negli ambienti mediterranei. Informatore Agrario 27, 2932.Google Scholar
Chevassus-Au-louis, B. & Bazile, D. (2008). Cultiver la diversité. Cahiers Agricultures 17, 7778.Google Scholar
Christensen, S. A., Pratt, D. B., Pratt, C., Nelson, P. T., Stevens, M. R., Jellen, E. N., Coleman, C. E., Fairbanks, D. J., Bonifacio, A. & Maughan, P. J. (2007). Assessment of genetic diversity in the USDA and CIP-FAO international nursery collections of quinoa (Chenopodium quinoa Willd.) using microsatellite markers. Plant Genetic Resources 5, 8295.Google Scholar
Cleveland, D. A., Soleri, D. & Smith, S. E. (1994). Do folk crop varieties have a role in sustainable agriculture? Bioscience 44, 740751.CrossRefGoogle Scholar
Cusack, D. F. (1984). Quinoa: grain of the Incas. Ecologist 14:2131.Google Scholar
DMCH (Dirección Meteorológica De Chile) (2011). Climas de Chile. Santiago, Chile: DMCH. Available online at: http://www.meteochile.gob.cl/climas/climas.html (verified 10 Jan 2012).Google Scholar
Ferguson, M. E., Jones, R. B., Bramel, P. J., Dominguez, C., Torre Do Vale, C. & Han, J. (2011). Post-flooding disaster crop diversity recovery: a case study of Cowpea in Mozambique. Disasters 36, 83100.Google Scholar
Forapani, S., Carboni, A., Paoletti, C., Moliterni, V. M. C., Ranalli, P. & Mandolino, G. (2001). Comparison of hemp varieties using random amplified polymorphic DNA markers. Crop Science 41, 16821689.Google Scholar
Fuentes, F. F. (2008). Mejoramiento Genético de la Quínoa. Revista Agricultura del Desierto 4, 7189.Google Scholar
Fuentes, F. & Bhargava, A. (2011). Morphological analysis of quinoa germplasm grown under lowland desert conditions. Journal of Agronomy and Crop Science 197, 124134.Google Scholar
Fuentes, F. F., Espinoza, P., Carevic, A., Von Baer, I., Soliai, M., Jellen, E. N. & Maughan, P. J. (2009 b). Chenopodium quinoa: Relaciones genéticas en los Andes de Sudamérica. In Anales VII Simposio de Recursos Genéticos para América Latina y el Caribe – SIRGEALC (Eds Seguel Benítez, I., León-Lobos, P., Piñera Vargas, J., Muñoz Vera, G. & Avendaño Fuentes, L.), Vol. 1, pp. 269270. Pucón, Chile: INIA, Ministerio de Agricultura.Google Scholar
Fuentes, F. F., Martínez, E. A., Hinrichsen, P. V., Jellen, E. N. & Maughan, P. J. (2009 c). Assessment of genetic diversity patterns in Chilean quinoa (Chenopodium quinoa Willd.) germplasm using multiplex fluorescent microsatellite markers. Conservation Genetics 10, 369377.CrossRefGoogle Scholar
Fuentes, F. F., Maughan, P. J. & Jellen, E. N. (2009 a). Diversidad genética y recursos genéticos para el mejoramiento de la quínoa (Chenopodium quinoa Willd). Revista Geográfica de Valparaíso 42, 2033.Google Scholar
de Haan, S. (2009). Potato diversity at height: multiple dimensions of farmer-driven in-situ conservation in the Andes. PhD thesis, Wageningen University, The Netherlands.Google Scholar
Hirose, Y., Fujita, T., Ishii, T. & Ueno, N. (2010). Antioxidative properties and flavonoid composition of Chenopodium quinoa seeds cultivated in Japan. Food Chemistry 119, 13001306.Google Scholar
INE (Instituto Nacional de Estadísticas) (2004). CHILE: Estimaciones y Proyecciones de Población por Sexo y Edad. País Urbano-Rural 1990–2020. Santiago, Chile: Instituto Nacional De Estadísticas. Available online at http://www.ine.cl/canales/chile_estadistico/demografia_y_vitales/demografia/demografia.php (verified 19 Dec 2011).Google Scholar
INE (Instituto Nacional de Estadísticas) (2007). Censo Agropecuario y Forestal 2007 Resultados por Comuna. Cuadro 7: Superficie Sembrada, Producción y Rendimiento de Cereales, Leguminosas y Tubérculos, en Riego y Secano, Según Región, Provincia y Especie. Santiago, Chile: Instituto Nacional De Estadísticas. Available online at: http://www.ine.cl/canales/chile_estadistico/censos_agropecuarios/censo_agropecuario_07_comunas.php (verified 10 January 2012).Google Scholar
INFOSTAT (2008). InfoStat Versión 2008. Córdoba, Argentina: Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.Google Scholar
Jacobsen, S. E. (2003). The worldwide potential of quinoa (Chenopodium quinoa Willd.). Food Review International 19, 167177.Google Scholar
Jacobsen, S. E., Mujica, A. & Jensen, C. R. (2003). The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Review International 19, 99109.Google Scholar
Jarvis, D. E., Kopp, O. R., Jellen, E. N., Mallory, M. A., Pattee, J., Bonifacio, A., Coleman, C. E., Stevens, M. R., Fairbanks, D. J. & Maughan, P. J. (2008). Simple sequence repeat marker development and genetic mapping in quinoa (Chenopodium quinoa Willd.). Journal of Genetics 87, 3951.CrossRefGoogle ScholarPubMed
Jellen, E. N., Kolano, B. A., Sederberg, M. C., Bonifacio, A. & Maughan, P. J. (2011). Chenopodium. In Wild Crop Relatives: Genomic and Breeding Resources (Ed. Kole, C.), pp. 3561. Berlin: Springer.Google Scholar
Lodhi, M. A., Yen, G. N., Weeden, N. F. & Reisch, B. (1994). A simple and efficient method for DNA extraction from grapevine cultivars and vitis species. Plant Molecular Biology Report 12, 613.Google Scholar
Martínez, E. A., Bazile, D., Thomet, M., Delatorre, J., Salazar, E., León-Lobos, P., Von Baer, I. & Nuñez, L. (2010). Neo-liberalism in Chile and its impacts on agriculture and biodiversity conservation of quinoa: a lesson for strengthening and developing new partnerships. In Innovation and Sustainable Development in Agriculture and Food: ISDA 2010, Montpellier, France, 28 June–1 July 2010 (Eds Coudel, E., Devautour, H., Soulard, C. & Hubert, B.), pp. 111. Montpellier, France: ISDA. Available online at http://hal.archives-ouvertes.fr/hal-00523036/en/ (verified 19 Dec 2011).Google Scholar
Martínez, E. A., Delatorre, J. & Von Bae, I. (2007). Quínoa: las potencialidades de un cultivo sub-utilizado en Chile. Tierra Adentro (INIA) 75, 2427.Google Scholar
Martínez, E. A., Jorquera, C., Veas, E. & Chia, E. (2009 b). El futuro de la quínoa en la región árida de Coquimbo: Lecciones y escenarios a partir de una investigación sobre su biodiversidad en Chile para la acción con agricultores locales. Revista Geográfica de Valparaíso 42, 95111.Google Scholar
Martínez, E. A., Veas, E., Jorquera, C., San Martín, R. & Jara, P. (2009 a). Re-introduction of Chenopodium quinoa Willd. into arid Chile: Cultivation of two lowland races under extremely low irrigation. Journal of Agronomy and Crop Science 195, 110.Google Scholar
Mallory, M. A., Hall, R. V., Mcnabb, A. R., Pratt, D. B., Jellen, E. N. & Maughan, P. J. (2008). Development and characterization of microsatellite markers for the grain Amaranths. Crop Science 48, 10981106.Google Scholar
Marti, N. & Pimbert, M. (2007). Barter markets for the conservation of agro-ecosystem multi-functionality: the case of the chalayplasa in the Peruvian Andes. International Journal of Agricultural Sustainability 5, 5169.Google Scholar
Mason, S. L., Stevens, M. R., Jellen, E. N., Bonifacio, A. A., Fairbanks, D. J., Coleman, C. E., Mccarty, R. R., Rasmussen, A. G. & Maughan, P. J. (2005). Development and use of microsatellite markers for germplasm characterization in quinoa (Chenopodium quinoa Willd.). Crop Science 45, 16181630.Google Scholar
Matus, I. A. & Hayes, P. M. (2002). Genetic diversity in three groups of barley germplasm assessed by simple sequence repeats. Genome 45, 10951106.Google Scholar
Miller, M. P. (1997). Tools for Population Genetic Analyses (TFPGA) 1·3: A Windows Program for the Analysis of Allozyme and Molecular Population Genetic Data. Flagstaff, AZ: M. P. Miller. http://www.marksgeneticsoftware.net/tfpga.htm (verified 19 Dec 2011).Google Scholar
Mujica, A. (2004). La quínoa Indígena, Características e historia. In La Kinwa Mapuche, Recuperación de un Cultivo para la Alimentación (Eds Sepúlveda, J., Thomet I., M., Palazuelos F., P. & Mujica, A.), pp. 2242. Temuco, Chile: Fundación para la Innovación Agraria. Ministerio de Agricultura.Google Scholar
Mujica, A., Jacobsen, S. E., Izquierdo, J. & Marathee, J. P. (2001). Resultados de la Prueba Americana y Europea de la Quinua. Puno, Peru: FAO, UNA, CIP.Google Scholar
NATIONAL RESEARCH COUNCIL (NRC) (1989). Lost Crops of the Incas: Little-known Plants of the Andes with Promise for Worldwide Cultivation. Washington, DC: National Academy Press.Google Scholar
Nei, M. (1972). Genetic distance between populations. American Naturalist 106, 283292.Google Scholar
Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583590.Google Scholar
Núñez, L. C., Bazile, D., Chia, E., Hocdé, H., Negrete, J. & Martinez, E. A. (2010). Representaciones Sociales acerca de la Conservación de la Biodiversidad en el caso de Productores tradicionales de Chenopodium quinoa Willd del secano costero en las Regiones de O´Higgins y el Maule. In Anales de la Sociedad Chilena de Ciencias Geográficas (Ed. Ceorgudis Maya, B.), pp. 181187. Valdivia, Chile: Sociedad Chilena de Ciencias Geográficas.Google Scholar
Orabi, J., Backes, G., Wolday, A., Yahyaoui, A. & Jahoor, A. (2007). The horn of Africa as a centre of barley diversification and a potential domestication site. Theoretical and Applied Genetics 114, 11171127.Google Scholar
Ott, J. (1992). Strategies for characterizing highly polymorphic markers in human gene mapping. American Journal of Human Genetics 51, 283290.Google Scholar
Page, R. D. M. (2001). TreeView (Win32) ver. 1.6.5. Glasgow, UK: R. D. M. Page. Available online at http://taxonomy.zoology.gla.ac.uk/rod/treeview.html (verified 20 Dec 2011).Google Scholar
Pavlicek, A., Hrda, S. & Flegr, J. (1999). FreeTree – Freeware program for construction of phylogenetic trees on the basis of distance data and bootstrap/jackknife analysis of the tree robustness. Application in the RAPD analysis of the genus Frenkelia. Folia Biologica 45, 9799. Program available online at http://web.natur.cuni.cz/flegr/freetree.php (verified 20 Dec 2011).Google Scholar
Pérez, I. (2005). Curadoras de Semillas, Contribución del Conocimiento Tradicional al Manejo Descentralizado de la Biodiversidad. Publicación Semestral CETSUR 5. Tomé, Chile: CETSUR.Google Scholar
Pressoir, G. & Berthaud, J. (2004). Population structure and strong divergent selection shape phenotypic diversification in maize landraces. Heredity 92, 95101.CrossRefGoogle ScholarPubMed
Pulvento, C., Riccardi, M., Lavini, A., D'andria, R., Iafelice, G. & Marconi, E. (2010). Field trial evaluation of two Chenopodium quinoa genotypes grown under rain-fed conditions in a typical Mediterranean environment in south Italy. Journal of Agronomy and Crop Science 196, 407411.Google Scholar
Rana, T. S., Narzary, D. & Ohri, D. (2010). Genetic diversity and relationships among some wild and cultivated species of Chenopodium L. (Amaranthaceae) using RAPD and DAMD methods. Current Science 98, 840846.Google Scholar
Risi, J. C. & Galwey, N. W. (1984). The Chenopodium grains of the Andes: Inca crops for modern agriculture. Advances in Applied Biology 10, 145216.Google Scholar
Rojas, W. (2003). Multivariate analysis of genetic diversity of Bolivian quinoa germplasm. Food Review International 19, 923.Google Scholar
Ruiz-Carrasco, K. B., Antognoni, F., Coulibaly, A. K., Lizardi, S., Covarrubias, A., Martínez, E. A., Molina-Montenegro, M. A., Biondi, S., Zurita-Silva, A. (2011). Variation in salinity tolerance of four lowland genotypes of quinoa (Chenopodium quinoa Willd.) as assessed by growth, physiological traits, and sodium transporter gene expression. Plant Physiology and Biochemistry 49, 13331341.Google Scholar
Skøt, L., Humphreys, M. O., Armstead, I., Heywood, S., Skøt, K. P., Sanderson, R., Thomas, I. D., Chorlton, K. H. & Sackville Hamilton, N. R. (2005). An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.). Molecular Breeding 15, 233245.Google Scholar
Sperling, L., Cooper, H. D. & Remington, T. (2008). Moving towards more effective seed aid. Journal of Development Studies 44, 586612.Google Scholar
Staab, S. (2003). En Búsqueda de Trabajo. Migración Internacional de las Mujeres Latinoamericanas y Caribeñas. Bibliografía Seleccionada. Serie Mujer y Desarrollo N°51. Santiago, Chile: CEPAL-ECLAC-UN.Google Scholar
STATSOFT (2001). Statistica (data analysis software system), version 6. Tulsa, OK: StatSoft Inc. Available online at http://www.statsoft.com (verified 20 Dec 2011).Google Scholar
Subedi, A., Chaudhary, P., Baniya, B. K., Rana, R. B., Tiwari, R. K., Rijal, D. K., Sthapit, B. R. & Jarvis, D. I. (2003). Who maintains crop genetic diversity and how? Implications for on-farm conservation and utilization. Culture and Agriculture 25, 4150.Google Scholar
Tagle, M. B. & Planella, M. T. (2002). La Quínoa en la Zona Central de Chile, Supervivencia de una Tradición Prehispánica. Santiago, Chile: Editorial IKU.Google Scholar
Taran, P. A. & Geronimi, E. (2004). Globalización y migraciones laborales: importancia de la protección. Futuros. Revista Trimestral Latinoamericana y Caribeña de Desarrollo Sustentable 2(8). Available online at: http://www.revistafuturos.info/indices/indice_8_home.htm (verified 10 Jan 2012).Google Scholar
Vargas, A., Elzinga, D. B., Rojas-Beltran, J. A., Bonifacio, A., Geary, B., Stevens, M. R., Jellen, E. N. & Maughan, P. J. (2010). Development and use of microsatellite markers for genetic diversity analysis of cañahua (Chenopodium pallidicaule Aellen). Genetic Resources and Crop Evolution 58, 727739.Google Scholar
Vega-Gálvez, A., Miranda, M., Vergara, J., Uribe, E., Puente, L. & Martínez, E. A. (2010). Nutrition facts and functional potential of quinoa (Chenopodium quinoa Willd.), an ancient Andean grain: a review. Journal of the Science of Food and Agriculture 90, 25412547.Google Scholar
Wale, E. (2008). A study on financial opportunity costs of growing local varieties of sorghum in Ethiopia: Implications for on-farm conservation policy. Ecological Economics 64, 603610.Google Scholar
Wilson, H. D. (1990). Quinua and relatives (Chenopodium sect. Chenopodium subsect. Cellulata). Economic Botany 44, 92110.Google Scholar
Wood, D. & Lenné, J. M. (1997). The conservation of agrobiodiversity on-farm: questioning the emerging paradigm. Biodiversity and Conservation 6, 109129.Google Scholar
Woodhead, M., Russell, J., Squirrell, J., Hollingsworth, P. M., Mackenzie, K., Gibby, M. & Powell, W. (2005). Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions. Molecular Ecology 14, 16811695.CrossRefGoogle ScholarPubMed
Wright, S. (1951). The genetical structure of populations. Annals of Human Genetics 15, 323354.Google Scholar