Latitudinal structured populations of the Mexican wild squash Cucurbita argyrosperma subsp. sororia revealed by microsatellite markers
Francisco J. Balvino-Olvera A B C , Karman F. Sánchez-Gómez A B C , Jorge Arturo Lobo D , Germán Avila-Sakar A E , Rogelio Cruz-Reyes A F , Gumersindo Sánchez-Montoya A B , Yvonne Herrerías-Diego A C , Antonio González-Rodríguez A B and Mauricio Quesada A B G
+ Author Affiliations
- Author Affiliations
A Laboratorio Nacional de Análisis Síntesis Ecológica, Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia, Michoacán 58190, México.
B Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán 58190, México.
C Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Morelia, Michoacán 58030, México.
D Escuela de Biología, Universidad de Costa Rica, San Pedro, Costa Rica.
E Department of Biology, The University of Winnipeg, Winnipeg, Manitoba R3B2E9, Canada.
F Facultad en Desarrollo Sustentable, Campus Costa Grande, Universidad Autónoma de Guerrero, Carretera Federal Acapulco-Zihuatanejo km 106, Técpan de Galeana, Guerrero, 40900, México.
G Corresponding author. Email: mquesada@cieco.unam.mx
Crop and Pasture Science 68(9) 850-858 https://doi.org/10.1071/CP17341
Submitted: 15 September 2017 Accepted: 25 October 2017 Published: 15 November 2017
Abstract
Crop wild relatives represent an important agronomic resource for crop improvement and biodiversity conservation. The wild squash Cucurbita argyrosperma subsp. sororia. (Cucurbitaceae) has been considered the wild ancestor of cultivated forms of C. argyrosperma. In order to characterise the geographic patterns of genetic variation in this wild cucurbit and to identify priority areas for conservation, we analysed the genetic diversity and structure of natural populations along the Mexican Pacific coast. By using 14 polymorphic microsatellites, we genotyped 378 individuals sampled from 61 locations. Standard population genetics analyses and group testing were conducted on the genotypes with the aid of principal coordinate analysis and Bayesian analysis. Overall, we found an average of 12.3 alleles per locus and an expected heterozygosity of 0.756. We found greater genetic diversity in southern populations. The fixation index was 0.113, suggesting a mixed mating system. The Mantel test revealed a minor distance effect on genetic differentiation between individuals (r = 0.321). Finally, we found three main groups of populations arranged in a mostly latitudinal pattern, from Sinaloa (north-west) to Oaxaca–Guerrero (south-east). The greater genetic diversity and heterogeneity among southern populations (Guerrero–Oaxaca), suggests that this region is an important centre of diversity of this wild squash with important implications for conservation.
Additional keywords: gene flow, genetic structure, plant mating systems, plant reproduction, SSR’s, wild and cultivated species, wild gourds.
References
Aguilar-Meléndez A, Morrell PL, Roose ML, Kim S-C (2009) Genetic diversity and structure in semiwild and domesticated chiles (Capsicum annuum; Solanaceae) from Mexico. American Journal of Botany 96, 1190–1202.| Genetic diversity and structure in semiwild and domesticated chiles (Capsicum annuum; Solanaceae) from Mexico.Crossref | GoogleScholarGoogle Scholar |
Bitocchi E, Nanni L, Bellucci E, Rossi M, Giardini A, Zeuli PS, Logozzo G, Stougaard J, McClean P, Attene G, Papa R (2012) Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proceedings of the National Academy of Sciences of the United States of America 109, E788–E796.
| Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlslCms74%3D&md5=db213d1055dae37e36d7177de4301738CAS |
Brush S, Kesseli R, Ortega R, Cisneros P, Zimmerer K, Quiros C (1995) Potato diversity in the Andean Center of Crop Domestication. Conservation Biology 9, 1189–1198.
| Potato diversity in the Andean Center of Crop Domestication.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=62715fe70f55a1e8368cb19a2e099e59CAS |
Ceballos G, Valenzuela D (2010) Diversidad ecología y conservación de vertebrados de Latinoamérica. In ‘Diversidad, amenazas y áreas prioritarias para la conservación de las selvas secas del Pacífico Mexicano’. (Eds G Ceballos, L Martínez, A García, E Espinoza, J Bezaury, R Dirzo) pp. 93–119. (Fondo de Cultura Económica: México, DF)
Cruz-Reyes R, Ávila-Sakar G, Sánchez-Montoya G, Quesada M (2015) Experimental assessment of gene flow between transgenic squash and a wild relative in the center of origin of cucurbits. Ecosphere 6, art248
| Experimental assessment of gene flow between transgenic squash and a wild relative in the center of origin of cucurbits.Crossref | GoogleScholarGoogle Scholar |
Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.
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=3c163868b2976bb3c0e90657373a96cdCAS |
Ferrari MJ, Stephenson AG, Mescher MC, Moraes CMD (2006) Inbreeding effects on blossom volatiles in Cucurbita pepo subsp. texana (Cucurbitaceae). American Journal of Botany 93, 1768–1774.
| Inbreeding effects on blossom volatiles in Cucurbita pepo subsp. texana (Cucurbitaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFGmtQ%3D%3D&md5=8fdc819c6c61695bc1c6884018459343CAS |
Ferriol M, Pico B (2008) ‘Vegetables I—Asteraceae, Brassicaceae.’ (Ed. J Prohens-Tomás, F Nuez) (Springer-Verlag)
Giannini TC, Lira-Saade R, Ayala R, Saraiva AM, Alves-dos-Santos I (2011) Ecological niche similarities of Peponapis bees and non-domesticated Cucurbita species. Ecological Modelling 222, 2011–2018.
| Ecological niche similarities of Peponapis bees and non-domesticated Cucurbita species.Crossref | GoogleScholarGoogle Scholar |
Gong L, Stift G, Kofler R, Pachner M, Lelley T (2008) Microsatellites for the genus Cucurbita and an SSR-based genetic linkage map of Cucurbita pepo L. Theoretical and Applied Genetics 117, 37–48.
| Microsatellites for the genus Cucurbita and an SSR-based genetic linkage map of Cucurbita pepo L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlWisbc%3D&md5=092dcd8995b2c800d294025ee0c0de54CAS |
Gonzáles Castro M, Palacios-Rojas N, Espinoza Banda A, Beyoda Salazar CA (2013) Diversidad genética en maíces nativos mexicanos tropicales. Revista Fitotecnia Mexicana 36, 239–338.
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 351, 1291–1298.
| Effects of life history traits on genetic diversity in plant species.Crossref | GoogleScholarGoogle Scholar |
Hayes CN, Winsor JA, Stephenson AG (2005) A comparison of male and female responses to inbreeding in Cucurbita pepo subsp. texana (Cucurbitaceae). American Journal of Botany 92, 107–115.
| A comparison of male and female responses to inbreeding in Cucurbita pepo subsp. texana (Cucurbitaceae).Crossref | GoogleScholarGoogle Scholar |
Hurd PJ, Linsley EG, Whitaker TW, Hurd PJ, Linsley EG, Whitaker TW (1970) Squash and gourd bees (Peponapis, Xenoglossa) and the origin of the cultivated Cucurbita. Evolution 25, 218–234.
Kirkpatrick KJ, Wilson HD (1988) Interspecific gene flow in Cucurbita: C. texana vs. C. pepo. American Journal of Botany 75, 519–527.
| Interspecific gene flow in Cucurbita: C. texana vs. C. pepo.Crossref | GoogleScholarGoogle Scholar |
Kohn JR, Biardi JE (1995) Outcrossing rates and inferred levels of inbreeding depression in gynodioecious Cucurbita foetidissima (Cucurbitaceae). Heredity 75, 77–83.
| Outcrossing rates and inferred levels of inbreeding depression in gynodioecious Cucurbita foetidissima (Cucurbitaceae).Crossref | GoogleScholarGoogle Scholar |
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 |
Lira R, Caballero J (2002) Ethnobotany of the wild Mexican Cucurbitaceae. Economic Botany 56, 380–398.
| Ethnobotany of the wild Mexican Cucurbitaceae.Crossref | GoogleScholarGoogle Scholar |
Lira R, Montes-Hernández E (1992) Cucurbits. In ‘Neglected crops: 1492 from a different perspective’. Vol. 26. (Eds JEH Bermejo, J León) pp. 63–67. (Food and Agriculture Organization of the United Nations: Rome)
Lira Saade R (1995) ‘Estudios taxonómicos y ecogeográficos de las Cucurbitaceae latinoamericanas de importancia económica.’ (Instituto de Biología, UNAM/International Plant Genetic Resources Institute: México, DF/Rome)
Loveless M, Hamrick J (1984) Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15, 65–95.
| Ecological determinants of genetic structure in plant populations.Crossref | GoogleScholarGoogle Scholar |
Mariano N, Dirzo R (2002) Cucurbita argyrosperma spp. sororia (LH Bailey) Merrick and Bates (Cucurbitaceae), Agüichichi. In ‘Historia natural de chamela’. (Eds F. Noguera-Martínez, J. Vega-Rivera, AN García-Aldrete and M. Quesada-Avendaño) pp. 167–170. (Instituto de Biología, UNAM: México, DF)
Matsuoka Y, Vigouroux Y, Goodman MM, Jesus Sanchez G, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the National Academy of Sciences 99, 6080–6084.
| A single domestication for maize shown by multilocus microsatellite genotyping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslWnsr8%3D&md5=e9e4d901b2bdd61cec2fe6a5a5b6f900CAS |
Merrick LC (1990) Systematics and evolution of a domesticated squash, Cucurbita argyrosperma, and its wild and weedy relatives. In ‘Biology and utilization of the Cucurbitaceae’. (Eds DM Bates, RW Robinson, C Jeffrey) pp. 77–95. (Cornell University Press: Ithaca, NY, USA)
Montes-Hernández S, Eguiarte LE (2002) Genetic structure and indirect estimates of gene flow in three taxa of Cucurbita (Cucurbitaceae) in western Mexico. American Journal of Botany 89, 1156–1163.
| Genetic structure and indirect estimates of gene flow in three taxa of Cucurbita (Cucurbitaceae) in western Mexico.Crossref | GoogleScholarGoogle Scholar |
Nee M (1990) The domestication of Cucurbita (Cucurbitaceae). Economic Botany 44, 56–68.
| The domestication of Cucurbita (Cucurbitaceae).Crossref | GoogleScholarGoogle Scholar |
Nevo E (1998) Genetic diversity in wild cereals: regional and local studies and their bearing on conservation ex situ and in situ. Genetic Resources and Crop Evolution 45, 355–370.
| Genetic diversity in wild cereals: regional and local studies and their bearing on conservation ex situ and in situ.Crossref | GoogleScholarGoogle Scholar |
Olsen KM, Schaal BA (2001) Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication. American Journal of Botany 88, 131–142.
| Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbktVSmsA%3D%3D&md5=b8d4a05e2c414df2697803bf41603184CAS |
Ortega J, Tschapka M, González-Terrazas TP, Suzán G, Medellín RA (2009) Phylogeography of Musonycteris harrisoni along the Pacific Coast of Mexico. Acta Chiropterologica 11, 259–269.
| Phylogeography of Musonycteris harrisoni along the Pacific Coast of Mexico.Crossref | GoogleScholarGoogle Scholar |
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=be52e75b4d8c1fb0d8e6a0622234ede0CAS |
Pope KO, Pohl MED, Jones JG, Lentz DL, von Nagy C, Vega FJ, Quitmyer IR (2001) Origin and environmental setting of ancient agriculture in the lowlands of Mesoamerica. Science 292, 1370–1373.
| Origin and environmental setting of ancient agriculture in the lowlands of Mesoamerica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVGjt7s%3D&md5=8ab7d557a7c43fc82fb221e66f72d08eCAS |
Pringle EG, Ramírez SR, Bonebrake TC, Gordon DM, Dirzo R (2012) Diversification and phylogeographic structure in widespread Azteca plant-ants from the northern Neotropics. Molecular Ecology 21, 3576–3592.
| Diversification and phylogeographic structure in widespread Azteca plant-ants from the northern Neotropics.Crossref | GoogleScholarGoogle Scholar |
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Sanjur OI, Piperno DR, Andres TC, Wessel-Beaver L (2002) Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: Implications for crop plant evolution and areas of origin. Proceedings of the National Academy of Sciences of the United States of America 99, 535–540.
| Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: Implications for crop plant evolution and areas of origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1CqtA%3D%3D&md5=fcc9e548ad2cacc0cbee795293063a2dCAS |
Smith BD (2005) Reassessing Coxcatlan Cave and the early history of domesticated plants in Mesoamerica. Proceedings of the National Academy of Sciences of the United States of America 102, 9438–9445.
| Reassessing Coxcatlan Cave and the early history of domesticated plants in Mesoamerica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVaksbw%3D&md5=356741146d117d0d6a0aa077f25a9cb1CAS |
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82, 561–573.
| Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure.Crossref | GoogleScholarGoogle Scholar |
Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel Test of Matrix Correspondence. Systematic Zoology 35, 627–632.
| Multiple regression and correlation extensions of the Mantel Test of Matrix Correspondence.Crossref | GoogleScholarGoogle Scholar |
Suárez-Atilano M, Burbrink F, Vázquez-Domínguez E (2014) Phylogeographical structure within Boa constrictor imperator across the lowlands and mountains of Central America and Mexico. Journal of Biogeography 41, 2371–2384.
| Phylogeographical structure within Boa constrictor imperator across the lowlands and mountains of Central America and Mexico.Crossref | GoogleScholarGoogle Scholar |
Vavilov NI, Dorofeev VF (1992) ‘Origin and geography of cultivated plants.’ (Cambridge University Press: Cambridge, UK)
Villand J, Skroch PW, Lai T, Hanson P, Kuo CG, Nienhuis J (1998) Genetic variation among tomato accessions from primary and secondary centers of diversity. Crop Science 38, 1339–1347.
| Genetic variation among tomato accessions from primary and secondary centers of diversity.Crossref | GoogleScholarGoogle Scholar |
Wessel-Beaver L (2000) Cucurbita argyrosperma sets fruits in fields where C. moschata is the only pollen source. Report – Cucurbit Genetics Cooperative 23, 62–63.
Wessel-Beaver L, Cuevas HE, Andres TC, Piperno DR (2004) Genetic compatibility between Cucurbita moschata and C. argyrosperma. In ‘Progress in cucurbit genetics and breeding research. Proceedings Cucurbitaceae 2004, the 8th EUCARPIA Meeting on Cucurbit Genetics and Breeding’. 12–17 July 2004. Olomouc, Czech Republic. pp. 393–400. (Palacký University: Olomouc, Czech Republic)
Zarza E, Reynoso VH, Emerson BC (2008) Diversification in the northern neotropics: mitochondrial and nuclear DNA phylogeography of the iguana Ctenosaura pectinata and related species. Molecular Ecology 17, 3259–3275.
| Diversification in the northern neotropics: mitochondrial and nuclear DNA phylogeography of the iguana Ctenosaura pectinata and related species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtValt7rJ&md5=da5a1d8cfa5c195b6baa6ad98d117429CAS |
Zarza E, Reynoso VH, Emerson BC (2011) Discordant patterns of geographic variation between mitochondrial and microsatellite markers in the Mexican black iguana (Ctenosaura pectinata) in a contact zone. Journal of Biogeography 38, 1394–1405.
| Discordant patterns of geographic variation between mitochondrial and microsatellite markers in the Mexican black iguana (Ctenosaura pectinata) in a contact zone.Crossref | GoogleScholarGoogle Scholar |
Zheng Y-H, Alverson AJ, Wang Q-F, Palmer JD (2013) Chloroplast phylogeny of Cucurbita: evolution of the domesticated and wild species. Journal of Systematics and Evolution 51, 326–334.
| Chloroplast phylogeny of Cucurbita: evolution of the domesticated and wild species.Crossref | GoogleScholarGoogle Scholar |
