Abstract
Theobroma grandiflorum (cupuassu) is an important fruit tree native to the Brazilian Amazon. Establishing the genetic diversity and structure of populations is critical to define long-term strategies for cupuassu conservation presently threatened by rapid deforestation. Three natural populations collected at the putative center of diversity, three groups of accessions established at a germplasm collection, and one derived from commercial plantings were analyzed. The genetic diversity was assessed using 21 polymorphic microsatellite loci originally developed for Theobroma cacao, disclosing a total of 113 alleles. The estimated genetic diversity parameters averaged over cupuassu populations (A = 3.53 alleles per locus; H e = 0.426; H o = 0.346) were lower than the values reported for other Neotropical tree species. The three natural populations presented a positive and significant fixation index (f), ranging from 0.133 to 0.234. Cupuassu apparently adhered to a general pattern of genetic diversity structure of some Neotropical tree species occurring at low densities, with a low intrapopulation genetic diversity and important levels of endogamy, possibly due to biparental inbreeding derived from the presence of spatial genetic structure in the populations. A high level of genetic divergence was detected among the natural populations (θ p = 0.301), a strong differentiation caused by limited gene flow, and suggesting that human interference in spreading and/or stimulating plantings might have had a smaller effect than expected. The approximate location of the T. grandiflorum center of diversity could not be confirmed by analyzing natural populations from the putative region.
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References
Adams WT (1981) Population genetics and gene conservation in Pacific Northwest conifers. In: Scudder GGE, Revel JL (eds) Evolution today. Proceedings of the 2nd International Congress of Systematic and Evolution Biology. Hunt Institute for Botanical Documentation, Carnegie-Mellon University, Pittsburgh, PA, USA, pp 401–415
Alves RM, Araújo DG, Fernandes JRQ (1997) Compatibilidade entre clones de cupuaçuzeiro (Theobroma grandiflorum). Rev Bras Genet 20(3):148 (abstract)
Alves RM, Artero AS, Sebbenn AM, Figueira A (2003) Mating system in a natural population of Theobroma grandiflorum (Willd. Ex Spreng.) Schum., by microsatellite markers. Genet Mol Biol 26:373–379
Alves RM, Sebbenn AM, Artero AS, Figueira A (2006) Microsatellite loci transferability from Theobroma cacao to Theobroma grandiflorum. Mol Ecol Notes 6:583–586
Azevedo VCR, Vinson CC, Ciampi AY (2005) Twelve microsatellite loci in Manilkara huberi (Ducke) Standl (Sapotaceae), an Amazonian timber species. Mol Ecol Notes 5:13–15
Brondani RPV, Zucchi MI, Brondani C, Rangel PHN, Borba TCO, Rangel PN, Magalhães MR, Vencovsky R (2005) Genetic structure of wild rice Oryza glumaepatula populations in three Brazilian biomes using microsatellite markers. Genetica 125:115–123
Brown AHD, Hardner CM (2000) Sampling the gene pools of forest trees for ex situ conservation. In: Young A, Boshier D, Boyle T (eds) Forest conservation genetics: Principles and practice. CSIRO, Australia, pp 183–196
Chase MR, Moller C, Kesseli R, Bawa KS (1996) Distant gene flow in tropical tree. Nature 383:398–399
Clement CR (1999) 1492 and the loss of Amazonian crop genetic resources. I. The relation between domestication and human population decline. Econ Bot 53:188–202
Cockerham CC, Weir BS (1993) Estimation of gene flow from F-statistics. Evolution 47:855–863
Collevatti RG, Grattapaglia D, Hay JD (2001a) Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Mol Ecol 10:349–356
Collevatti RG, Grattapaglia D, Hay JD (2001b) High resolution microsatellite based analysis of the mating system allows the detection of significant biparental inbreeding in Caryocar brasiliensis, and endangered tropical tree species. Heredity 86:60–67
Cope FW (1962) The mechanism of pollen incompatibility in Theobroma cacao. Heredity 17:157–182
Cope FW (1976) Cacao, Theobroma cacao. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 285–289
Creste S, Tulmann-Neto A, Figueira A (2001) Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306
Crow JF, Aoki K (1984) Group selection for a polygenic behavioural trait: estimating the degree of population subdivision. Proc Natl Acad Sci USA 81:6073–6077
Cuatrecasas JA (1964) Cocoa and its allies: a taxonomic revision of the genus Theobroma. Contrib US Natl Herb 35(6):32–46
Dayanandan S, Bawa KS, Kesseli R (1999) Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae). Mol Ecol 8:1585–1592
Degen B (2006) Genetic data analysis and numerical test. GDA-NT. Beta version 1.0
Degen B, Bandou E, Caron H (2004) Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana. Heredity 93:585–591
Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12:753–764
Ducke A (1946) Plantas de cultura precolombiana na Amazônia Brasileira: notas sobre as espécies ou formas espontâneas que supostamente lhes teriam dado origem. Boletim Técnico, 8, 24 p. Belém, IAN, Brazil
Dutech C, Joly HI, Jarner P (2004) Gene flow, historical population dynamics and genetic diversity within French Guiana populations of a rainforest tree species, Vouacapoua americana. Heredity 92:69–77
Falcão MA, Lleras E (1983) Aspectos fenológicos ecológicos e de produtividade do cupuaçu, Theobroma grandiflorum (Willd ex Spreng) Schum. Acta Amazonica 13(5–6):725–735
Gilabert-Escrivá MV, Gonçalves LAG, Figueira A, Silva CRS (2002) Fatty acid and triacylglycerol composition and thermal behavior of fats from seeds of Brazilian Amazonian Theobroma species. J Sci Food Agric 82:1425–1431
Glendinning DR (1960) Selfing of self-incompatible cocoa. Nature 187:170
Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier MH, Doligez A, Dutech C, Kremer A, Latouche-Hallé C, Troispoux V, Veron V, Degen B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571
Hollingsworth PM, Dawson IK, Goodall-Copestake WP, Richardson JE, Weber JC, Sotelo-Montes C, Pennington RT (2005) Do farmers reduce genetic diversity when they domesticate tropical trees? A case study from Amazonia. Mol Ecol 14:497–501
Homma AKO, Walker RT, Carvalho RA, Conto AJ, Ferreira CAP (1996) Razões de risco e rentabilidade na destruição de recursos florestais: o caso de castanhais em lotes de colonos no Sul do Pará. Rev Econômica do Nordeste 27(3):515–535
Knight R, Rogers H (1955) Incompatibility in Theobroma cacao. Heredity 9:67–69
Lanaud C, Risterucci AM, Pieretti I, Falque M, Bouet A, Lagoda PJL (1999) Isolation and characterization of microsatellites in Theobroma cacao L. Mol Ecol 8:2141–2143
Latouche-Hallé C, Ramboer A, Bandou E, Caron H, Kremer A (2003) Nuclear and chloroplast genetic structure indicate fine-scale spatial dynamics in a neotropical tree population. Heredity 91:181–190
Latouche-Hallé C, Ramboer A, Bandou E, Caron H, Kremer A (2004) Long-distance pollen flow and tolerance to selfing in a neotropical tree species. Mol Ecol 13:1055–1064
Lemes MR, Gribel R, Proctor J, Grattapaglia D (2003) Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on variation at microsatellite loci: implications for conservation. Mol Ecol 12: 2875–2883
Lewis PO, Zaykin D (1999) GDA—Genetic date analysis: version 1.0 (d12) for Windows (software), 39 p. The University of New Mexico, Albuquerque, NM, USA. http://www.lewis.eeb.uconn.edu/lewishome/software.html
Lima RR, Costa JPC (1991) Registro de introduções de plantas de cultura pré-colombiana coletadas na Amazônia Brasileira. Série Documentos, 58, 191 p. Belém, Embrapa, Brazil
Manly BFJ (1997) Randomization, bootstrap and Monte Carlo Methods in biology. Chapman & Hall, London, UK
Miller MP (1997) Tools for Population Genetic Analyses (TFPGA) version 1.3: a windows program for the analysis of allozyme and molecular population genetic data©. Flagstaff Northern Arizona University, Flagstaff, AZ
Morand ME, Brachet S, Rossignol P, Dufour J, Frascaria-Lacoste N (2002) A generalized heterozygote deficiency assessed with microsatellites in French common ash populations. Mol Ecol 11:377–385
Motamayor JC, Risterucci AM, Lopez PA, Ortiz CF, Moreno A, Lanaud C (2002) Cacao domestication I: the origin of the cacao cultivated by the Mayas. Heredity 89:308–386
Namkoong G (1988) Sampling for germplasm collections. Hortscience 23:79–81
Nei M (1978) Estimation of average heterozygosity and genetic distance from small number of individuals. Genetics 89:583–590
N’Goran JAK, Laurent V, Risterucci AM, Lanaud C (2000) The genetic structure of cocoa (Theobroma cacao L.) populations revealed by RFLP analysis. Euphytica 115:83–90
Novick RR, Dick CW, Lemes MR, Navarro C, Caccone A, Bermingham E (2003) Genetic structure of Mesoamerican populations of big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Mol Ecol 12:2885–2893
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Ronning CM, Schnell RJ (1994) Allozyme diversity in a germplasm collection of Theobroma cacao L. J Hered 85:291–295
Rossetto M, Slade RW, Baverstock PR, Henry RJ, Lee LS (1999) Microsatellite variation and assessment of genetic structure in tea (Melaleuca alternifolia—Myrtaceae). Mol Ecol 8:633–643
Sanou H, Lovett PN, Bouvet JN (2005) Comparison of quantitative and molecular variation in agroforestry populations of the shea tree (Vitellaria paradoxa C.F. Geartn) in Mali. Mol Ecol 14:2601–2610
Seoane CES, Sebbenn AM, Kageyama PY (2001) Sistema de reprodução em populações de Esenbeckia leiocarpa Engl. Rev do Instituto Florestal 13(1):19–26
Sereno ML, Albuquerque PSB, Vencovsky R, Figueira A (2006) Genetic diversity and natural population structure of cacao (Theobroma cacao L.) from the Brazilian Amazon evaluated by microsatellite markers. Conserv Genet 6:13–24
Shepherd M, Cross M, Maguire TL, Dieters MJ, Williams CG, Henry RJ (2002) Transpecific microsatellites for hard pines. Theor Appl Genet 104:819–827
van Treuren K, Karkkainen H, Baena-Gonzalez K, Savolainen E (1997) Evolution of microsatellites in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana. Mol Biol Evol 14:220–229
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55
Velho CC, Whipkey A, Janick J (1990) Cupuassu: a new beverage crop for Brazil. In: Janick J, Simon JE (eds) Advances in new crops. Timber, Portland, OR, USA, pp 372–375
Ward M, Dick CW, Gribel R, Lowe AJ (2005) To self, or not to self: a review of outcrossing and pollen-mediated gene flow in neotropical trees. Heredity 95:246–254
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
White GM, Boshier DH, Powell W (1999) Genetic variation within a fragmented population of Swietenia humilis Zucc. Mol Ecol 8:1899–1909
Zucchi MI, Brondani RP, Pinheiro JB, Chaves LJ, Coelho AS, Vencovsky R (2003) Genetic structure and gene flow in Eugenia dysenterica DC in the Brazilian Cerrado utilizing SSR markers. Genet Mol Biol 26:449–457
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We would like to thank for the financial support from the Brazilian National Research Council (CNPq), International Foundation of Science (IFS), and FAPESP.
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Alves, R.M., Sebbenn, A.M., Artero, A.S. et al. High levels of genetic divergence and inbreeding in populations of cupuassu (Theobroma grandiflorum). Tree Genetics & Genomes 3, 289–298 (2007). https://doi.org/10.1007/s11295-006-0066-9
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DOI: https://doi.org/10.1007/s11295-006-0066-9