Abstract
Little is known regarding the effect of fragmentation and human agricultural management on the genetic variation and gene flow of Cucurbita pepo L., 1753 in moderate fragmented areas in central Guatemala. We hypothesize that the genetic variation of C. pepo is affected by forest fragmentation and by traditional agricultural management. Therefore, we aim to determine: (1) the genetic diversity and genetic structure of C. pepo in the Cloud Forest Corridor (CFC) (2) the extent of genetic admixture between commercial variety (CV) and traditional landraces (TL) of C. pepo, (3) the effect of habitat fragmentation in the population genetics of C. pepo with a landscape approach, and (4) the potential relationship between traditional management practices and genetic diversity of C. pepo in the CFC. We detected the existence of high level of genetic diversity (AR = 3.43; He = 0.50), inbreeding (Fis = 0.25) and moderate population structure of C. pepo in the CFC (Fst = 0.16). No correlation between landscape and genetics was found. Also, we found high genetic admixture between CV and TL. It seems that human practices, mainly related with seed exchange patterns, could affect genetic diversity of C. pepo in the CFC. C. pepo populations in the CFC are structured, with inbreeding, and show admixture with the CV, an aspect that could affect its genetic diversity. The agricultural management influenced the population genetics of C. pepo in the CFC, but the landscape did not. We suggest that special efforts should be made to preserve the diversity of this important indigenous food source for Guatemalan people as well as their management practices.
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References
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980. https://doi.org/10.1111/j.1461-0248.2006.00927.x
Aguilar R, Quesada M, Ashworth L et al (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. https://doi.org/10.1111/j.1365-294X.2008.03971.x
Ahrens CW, James EA (2016) Conserving the small milkwort, Comesperma polygaloides, a vulnerable subshrub in a fragmented landscape. Conserv Genet 17:891–901. https://doi.org/10.1007/s10592-016-0830-9
Barbieri RL, Gomes JCC, Alercia A, Padulosi S (2014) Agricultural biodiversity in southern Brazil: integrating efforts for conservation and use of neglected and underutilized species. Sustain 6:741–757. https://doi.org/10.3390/su6020741
Barnaud A, Deu M, Garine E et al (2007) Local genetic diversity of sorghum in a village in northern Cameroon: structure and dynamics of landraces. Theor Appl Genet 114:237–248. https://doi.org/10.1007/s00122-006-0426-8
Bellon MR (1996) The dynamics of crop infraspecific diversity: a conceptual framework at the farmer level 1. Econ Bot 50:26–39. https://doi.org/10.1007/BF02862110
Bisognin DA (2002) Origin and evolution of cultivated cucurbits. Ciência Rural 32:715–723. https://doi.org/10.1590/S0103-84782002000400028
Campbell JA, Vannini JP (1989) Distribution of amphibians and reptiles in Guatemala and Belize. Proc West Found Vert Zool 4:1–21
Casas A, Otero-Arnaiz A, Pérez-Negrón E, Valiente-Banuet A (2007) In situ management and domestication of plants in Mesoamerica. Ann Bot 100:1101–1115. https://doi.org/10.1093/aob/mcm126
CECON (2000) Plan maestro 2000–2004 Biotopo Universitario “Mario Dary Rivera” para la conservación del Quetzal. In: Guatemala: Centro de Estudios Conservacionistas (CECON), Universidad de San Carlos de Guatemala (USAC), p 119
Crawley M (ed) (2007) Mixed-effects models. In: The R book. Wiley, West Sussex, p 627
Decker-Walters DS, Walters TW (1990) Genealogy and gene flow among annual domesticated species of Cucurbita. Can J Bot 68:782–789. https://doi.org/10.1139/b90-104
Doyle J, Doyle J (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem Bull 19:11–15
Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
Enriquez E, Ayala R, Gonzalez VH, Núñez-Farfan J (2015) Alpha and beta diversity of bees and their pollination role on Cucurbita pepo L. (Cucurbitaceae) in the Guatemalan cloud forest. Pan-Pac Entomol 91:211–222
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. https://doi.org/10.1007/s00424-009-0730-7
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166
Galluzzi G, López I (2014) Conservation and use of genetic resources of underutilized crops in the Americas—a continental analysis. Sustain 6:980–1017. https://doi.org/10.3390/su6020980
García B (1999) El Biotopo Universitario para la Conservación del Quetzal “Mario Dary Rivera”. Revista Mesoamericana 4(2):53–54
Gong L, Pachner M, Kalai K, Lelley T (2008) SSR-based genetic linkage map of Cucurbita moschata and its synteny with Cucurbita pepo. Genome 51:878–887. https://doi.org/10.1139/G08-072
Gong L, Paris HS, Stift G, Lelley T (2013) Genetic relationships and evolution in Cucurbita as viewed with simple sequence repeat polymorphisms: the centrality of C. okeechobeensis. Genet Resour Crop Evol 60:1531–1546. https://doi.org/10.1007/s10722-012-9940-5
González-Jara P, Moreno-Letelier A, Fraile A et al (2011) Impact of human management on the genetic variation of wild pepper Capsicum annuum var. glabriusculum. PLoS ONE 6(12):e28715. https://doi.org/10.1371/journal.pone.0028715
Hamrick JL, Godt MJW (1997) Allozyme diversity in cultivated crops. Crop Sci 37(1):26–30
Hulce D, Li X, Snyder-Leiby T (2011) GeneMarker Genotyping software: tools to increase the statistical power of DNA fragment analysis. J Biomol Tech 22:S35–S36
Instituto Nacional de Estadística -INE- (2002) Censo Nacional Agropecuario. Guatemala
Isac SA, Breno M, Walters FS (2016) Pollination in cucurbit crops. In: Mohammad P (ed) Handbook of cucurbits, growth, cultural practices, and physiology. CRC Press, London, pp 181–200
Jaffé R, Castilla A, Pope N, Imperatriz-Fonseca VL, Metzger JP, Arias MC, Jha S (2016) Landscape genetics of a tropical rescue pollinator. Conserv Genet 16:267–278
Jarvis DI, Brown AHD, Cuong PH 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. https://doi.org/10.1073/pnas.0800607105
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13
Johannessen CL (1982) Domestication process of maize continues in Guatemala. Econ Bot 36:84–99. https://doi.org/10.1007/BF02858703
Johannessen CL, Wilson MR, Davenport WA (1970) The domestication of maize: process or event? Geogr Rev 60:393–413
Kirkpatrick KJ, Wilson HD (1988) Interspecific gene flow in Cucurbita: C. texana vs. C. pepo. Am J Bot 75:519. https://doi.org/10.2307/2444217
Landaverde-González P, Enríquez E, Ariza MA, Murray T, Paxton RJ, Husemann M (2017) Fragmentation in the clouds? The population genetics of the native bee Partamona bilineata (Hymenoptera: Apidae: Meliponini) in the cloud forests of Guatemala. Conserv Genet 18:631–643
Lira R, Rodriguez-Jimenez C, Alvarado JL et al (1998) Diversidad e importancia de la familia Cucurbitaceae en México. Acta Bot Mex 42:43–77
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Martínez-Castillo J, Colunga-García MP, 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 55:1065–1077. https://doi.org/10.1007/s10722-008-9314-1
Meléndez-Ramirez V, Magaña-Rueda S, Parra-Tabla V, Ayala R, Navarro J (2002) Diversity of native bee visitors of cucurbit crops (Cucurbitaceae) in Yucatán, México. J Insect Conserv 6(3):135–147
Merrick LC (1995) Squashes, pumpkins and gourds: Cucurbita (Cucurbitaceae). In: Smartl J, Simmonds NW (eds) Evolution of Crop Plants, 2nd edn. Longman Scientific & Technical, Harlow, pp 95–105
Miller MP (1997) Tools for population genetic analyses (TFPGA) V. 1.3. Departament of Biological science. Northern Arizona University, USA, p 33
Montes-Hernández S, Eguiarte L (2002) Genetic structure and indirect estimates of gene flow in three taxa of Cucurbita (Curbitaceae) in Western México. Am J Bot 89:1156–1163
Montes-Hernández S, Merrick LC, Eguiarte LE (2005) Maintenance of squash (Cucurbita spp.) landrace diversity by farmers’ activities in Mexico. Genet Resour Crop Evol 52:697–707. https://doi.org/10.1007/s10722-003-6018-4
Mujaju C, Sehic J, Werlemark G et al (2010) Genetic diversity in watermelon (Citrullus lanatus) landraces from Zimbabwe revealed by RAPD and SSR markers. Hereditas 147:142–153. https://doi.org/10.1111/j.1601-5223.2010.02165.x
Mutegi E, Sagnard F, Semagn K et al (2011) Genetic structure and relationships within and between cultivated and wild sorghum (Sorghum bicolor (L.) Moench) in Kenya as revealed by microsatellite markers. Theor Appl Genet 122:989–1004. https://doi.org/10.1007/s00122-010-1504-5
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155. https://doi.org/10.1111/j.1365-294X.2004.02141.x
Ordóñez N (1999) Diversidad de Mamíferos Menores en Cuatro Bosques Nubosos del Núcleo de Centroamérica. Tesis de licenciatura en Biología, Universidad de San Carlos de Guatemala, Guatemala, p 71
Paris HS (2016) Germplasm enhancement of Cucurbita pepo (pumpkin, squash, gourd: Cucurbitaceae): progress and challenges. Euphytica 208:415–438. https://doi.org/10.1007/s10681-015-1605-y
Paris HS, Yonash N, Portnoy V et al (2003) Assessment of genetic relationships in Cucurbita pepo (Cucurbitaceae) using DNA markers. Theor Appl Genet. https://doi.org/10.1007/s00122-002-1157-0
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
Perales HR, Benz BF, Brush SB (2005) Maize diversity and ethnolinguistic diversity in Chiapas, Mexico. Proc Natl Acad Sci USA 102:949–954. https://doi.org/10.1073/pnas.0408701102
Pinheiro J, Bates D, Sarkar D, R Core-Team (2016) nlme: linear and nonlinear mixed effects models. In: R package version, 3-1-125 ed. http://CRAN.R-project.org/package=nime
Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503
Pressoir G, Berthaud J (2004) Patterns of population structure in maize landraces from the Central Valleys of Oaxaca in Mexico. Heredity 92:88–94
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Development Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Viena
Rarmond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
RECOSMO (2007) Proyecto Región de Conservación y Desarrollo Sostenible Sarstún-Motagua–RECOSMO. In: Creación de una red ambientalista regional en Guatemala. Guatemala, p 214
Rios H, Fernandez A, Batista O (1997) Cuban pumpkin genetic variability under low input conditions. Cucurbit Genet Coop Rep 20:48–49
Schuster JC, Cano EB, Cardona C (2000) Un método sencillo para priorizar la conservación de los bosques nubosos de Guatemala, usando passalidae (coleoptera) como organismos indicadores. Acta Zool Mex 80:197–209
SEGEPLAN (2010) Secretaría General de Planificación–SEGEPLAN-. Plan de Desarrollo Municipal del Municipio de Salamá, Baja Verapaz, Guatemala 2011–2015
SEGEPLAN (2011) Secretaría General de Planificación–SEGEPLAN-. Plan de Desarrollo Municipal del Municipio de Purulhá, Baja Verapaz, Guatemala 2011–2015
Slaa JE, Chaves LAS, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315
Tang H, Sezen U, Paterson AH (2010) Domestication and plant genomes. Curr Opin Plant Biol 13:160–166. https://doi.org/10.1016/j.pbi.2009.10.008
Turner BL II, Miksicek CH (1984) Economic plant species associated with prehistorical agriculture in the maya lowlands. Econ Bot 38:179–193
Van Etten J, de Bruin S (2007) Regional and local maize seed exchange and replacement in the western highlands of Guatemala. Plant Genet Resour 5:57–70. https://doi.org/10.1017/S147926210767230X
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 4:535–538
Vavilov NI (1951) The origin, variation, immunity and breeding of cultivated plants. Chron Bot 13:6–366
Vigouroux Y, Barnaud A, Scarcelli N, Thuillet AC (2011) Biodiversity, evolution and adaptation of cultivated crops. C R Biol 334:450–457. https://doi.org/10.1016/j.crvi.2011.03.003
Wessel-Beaver L (1998) Pumpkin breeding with a tropical twist. Cucurbit Netw News 5:2–3
Williams-Linera G (1997) Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Glob Ecol Biogeogr Lett 6:115–127. https://doi.org/10.2307/2997568
Wilson G, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420
Ximenez F (1967) Historia Natural del Reino de Guatemala. Editorial José de Pineda Ibarra, Guatemala, p 351
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Zizumbo-Villarreal D, Colunga-García MP, Payró E et al (2005) Population structure and evolutionary dynamics of wild-weedy-domesticated complexes of common bean in a Mesoamerican region. Crop Sci 45:1073–1083. https://doi.org/10.2135/cropsci2004.0304
Acknowledgements
We are grateful to Dr. Carlota Monroy and Dr. Ricardo Ayala, members of the Ph. D. Advisor Committee of E.E. for their guidance during her studies. Thanks to the administrative staff and the forest guard of the Quetzal Conservation Biotope in Baja Verapaz, Guatemala. Dr. M. Quesada kindly provided two of the microsatellite’s primers used in this study (CMTp 201 and CMTp 245; Project SEP-CONACYT 2009-131008). Dra. Laura Marquez Valdemar, Biology Institute, National Autonomous University of Mexico (UNAM) for her valuable help in genotyping. E.E. acknowledges the Graduate Program in Biological Sciences of the National Autonomous University of Mexico (UNAM). Financial support for this project was provided by the Science and Technology National Fund of Guatemala (FODECYT 15-2011) granted to E.E. Enríquez; and from the Laboratory of Ecological Genetics and Evolution, Institute of Ecology, National Autonomous University of Mexico UNAM.
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Enríquez, E., Landaverde-González, P., Lima-Cordón, R. et al. Population genetics of traditional landraces of Cucurbita pepo L., 1753 in the cloud forest in Baja Verapaz, Guatemala. Genet Resour Crop Evol 65, 979–991 (2018). https://doi.org/10.1007/s10722-017-0589-y
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DOI: https://doi.org/10.1007/s10722-017-0589-y