Present Spatial Diversity Patterns of Theobroma cacao L. in the Neotropics Reflect Genetic Differentiation in Pleistocene Refugia Followed by Human-Influenced Dispersal

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Thomas, Evert ^a   van Zonneveld, Maarten ^a,b   Loo, Judy ^c   Hodgkin, Toby ^c   Galluzzi, Gea ^a   van Etten, Jacob ^a  

^a Regional Office for the Americas   (Colombia)

^b GHENT UNIVERSITY   (Belgium)

^c Headquarters Bioversity International   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAZIL; CACAO; CLUSTER ANALYSIS; COLOMBIA; ECOLOGICAL NICHE; GENE CLUSTER; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; GERMPLASM; GLACIATION; NEOTROPICS; NONHUMAN; PERU; PLANT GENETICS; PLEISTOCENE; SEED DISPERSAL; SIMPLE SEQUENCE REPEAT; SOUTH AND CENTRAL AMERICA; SPECIES REFUGE;

BRAZIL; CACAO; CLUSTER ANALYSIS; COLOMBIA; GENETIC SPECIATION; GENETIC VARIATION; HUMANS; PERU; SOUTH AMERICA;

THEOBROMA CACAO;

EID: 84868148259     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047676     Document Type: Article

References (62)

1. Motamayor JC, Risterucci AM, Lopez PA, Ortiz CF, Moreno A, et al. (2002) Cacao domestication I: the origin of the cacao cultivated by the Mayas. Heredity 89: 380-386.
2. Loor RG, Risterucci AM, Courtois B, Fouet O, Jeanneau M, et al. (2009) Tracing the native ancestors of the modern Theobroma cacao L. population in Ecuador. Tree Genetics & Genomes 5: 421-433.
3. 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. Conservation Genetics 7: 13-24.
4. Lachenaud P, Zhang D, (2008) Genetic diversity and population structure in wild stands of cacao trees (Theobroma cacao L.) in French Guiana. Annals of Forest Science 65: 310.
5. Zhang D, Arevalo-Gardini E, Mischke S, Zúñiga-Cernades L, Barreto-Chavez A, et al. (2006) Genetic diversity and structure of managed and semi-natural populations of cocoa (Theobroma cacao) in the Huallaga and Ucayali Valleys of Peru. Annals of botany 98: 647-655.
6. Zhang D, Boccara M, Motilal L, Mischke S, Johnson ES, et al. (2009) Molecular characterization of an earliest cacao (Theobroma cacao L.) collection from Upper Amazon using microsatellite DNA markers. Tree Genetics & Genomes 5: 595-607.
7. Zhang D, Martínez WJ, Johnson ES, Somarriba E, Phillips-Mora W, et al. (2012) Genetic diversity and spatial structure in a new distinct Theobroma cacao L. population in Bolivia. Genetic Resources and Crop Evolution 59: 239-252.
8. Trognitz B, Scheldeman X, Hansel-Hohl K, Kuant A, Grebe H, et al. (2011) Genetic population structure of cacao plantings within a young production area in Nicaragua. PloS ONE 6: e16056.
9. Motamayor JC, Lachenaud P, da Silva E Mota JW, Loor R, Kuhn DN, et al. (2008) Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PloS ONE 3: e3311.
10. Silva CRS, Albuquerque PSB, Ervedosa FR, Mota JWS, Figueira A, et al. (2011) Understanding the genetic diversity, spatial genetic structure and mating system at the hierarchical levels of fruits and individuals of a continuous Theobroma cacao population from the Brazilian Amazon. Heredity 106: 973-985.
11. Pautasso M, (2009) Geographical genetics and the conservation of forest trees. Perspectives in Plant Ecology, Evolution and Systematics 11: 157-189.
12. van Zonneveld M, Scheldeman X, Escribano P, Viruel MA, Van Damme P, et al. (2012) Mapping genetic diversity of cherimoya (Annona cherimola Mill.): application of spatial analysis for conservation and use of plant genetic resources. PLoS ONE 7: e29845.
13. van Etten J, Hijmans RJ, (2010) A geospatial modelling approach integrating archaeobotany and genetics to trace the origin and dispersal of domesticated plants. PLoS ONE 5: e12060.
14. Bush MB, (1996) Amazonian conservation in a changing world. Biological Conservation 76: 219-228.
15. Bush MB, Oliveira PED (2006) The rise and fall of the refugial hypothesis of Amazonian speciation: a paleoecological perspective. Biota Neotropica 6.
16. Haffer J, Prance GT, (2001) Climatic forcing of evolution in Amazonia during the Cenozoic: on the refuge theory of biotic differentiation. Amazoniana 16: 579-607.
17. Bonaccorso E, Koch I, Peterson AT, (2006) Pleistocene fragmentation of Amazon species' ranges. Diversity & Distributions 12: 157-164.
18. Mayle FE, Beerling DJ, Gosling WD, Bush MB, (2004) Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philosophical Transactions of the Royal Society of London Series B, Biological sciences 359: 499-514.
19. Beerling DJ, Mayle FE, (2006) Contrasting effects of climate and CO 2 on Amazonian ecosystems since the last glacial maximum. Global Change Biology 12: 1977-1984.
20. Pennington RT, Lavin M, Prado DE, Pendry CA, Pell SK, et al. (2004) Historical climate change and speciation: Neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 359: 359-537.
21. Stewart JR, Lister AM, Barnes I, Dalén L, (2010) Refugia revisited: individualistic responses of species in space and time. Proceedings of The Royal Society Biological sciences 277: 661-671.
22. Waltari E, Hijmans RJ, Peterson AT, Nyári AS, Perkins SL, et al. (2007) Locating pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PloS ONE 2: e563.
23. Shepard G, Ramirez H, (2011) "Made in Brazil": human dispersal of the Brazil Nut (Bertholletia excelsa, Lecythidaceae) in ancient Amazonia. Economic Botany 65: 44-65.
24. Clement CR, de Cristo-Araújo M, d'Eeckenbrugge GC, Alves Pereira A, Picanço-Rodrigues D, (2010) Origin and Domestication of Native Amazonian Crops. Diversity 2: 72-106.
25. Powis TG, Cyphers A, Gaikwad NW, Grivetti L, Cheong K, (2011) Cacao use and the San Lorenzo Olmec. Proceedings of the National Academy of Sciences of the United States of America 108: 8595-8600.
26. Motamayor, JC; Lanaud C (2002) Molecular analysis of the origin and domestication of Theobroma cacao L. In: Engels, JMM, Ramanatha Rao, V, Brown, AHD, Jackson MT, editors. Managing Plant Genetic Diversity. Rome. 77-87.
27. Patiño Rodriguez VM (2002) Historia y dispersión de los frutales nativos del Neotropico. Cali, Colombia: Centro Internacional de Agricultura Tropical.
28. Clement CR, (1999) 1492 and the loss of Amazonian crop genetic resources. II. Crop biogeography at contact. Economic Botany 53: 203-216.
29. Henderson JS, Joyce RA, Hall GR, Hurst WJ, McGovern PE, (2007) Chemical and archaeological evidence for the earliest cacao beverages. Proceedings of the National Academy of Sciences of the United States of America 104: 18937-18940.
30. Thomas E, (2012) The impact of traditional lifestyle, provenance and contact history on plant knowledge: a comparison of two small-scale societies from the Bolivian Amazon. Human Ecology 40: 355-368.
31. Guimaraes PR, Galetti M, Jordano P, (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE 3: e1745.
32. Hijmans RJ, Guarino L, Cruz M, Rojas E, (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127: 15-19.
33. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
34. Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 9, June 2008 [and more or less continuously updated since].
35. The Plant List (2010) Version 1. Published on the Internet. Available:http://www.theplantlist.org.
36. Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landscape Ecology: 797-807.
37. Frankel OH, Brown AHD, Burdon J (1995a) The genetic diversity of wild plants. In: The conservation of plant biodiversity. Cambridge, Great Britain: University Press. 10-38.
38. Nei M, (1973) Analysis of Gene Diversity in Subdivided Populations. Proceedings of the National Academy of Sciences 70: 3321-3323.
39. Leberg PL, (2002) Estimating allelic richness: effects of sample size. Molecular Ecology 11: 2445-2449.
40. Comps B, Go D, Petit RJ, (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European Beech. Genetics 157: 389-397.
41. R Development Core Team (2011) R: A language and environment for statistical computing. Version 2.14. R Foundation for Statistical Computing, Vienna, Austria.
42. Szpiech Z, Jakobsson M, Rosenberg N, (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498-2504.
43. Jombart T, Devillard S, Dufour A-B, Pontier D, (2008a) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101: 92-103.
44. Jombart T, (2008b) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405.
45. Jombart T (2011) A tutorial for Discriminant Analysis of Principal Components (DAPC) using adegenet 1.3-0. vignette for R package.
46. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, et al. (2011) vegan: Community Ecology Package. R package version 1.17-12.
47. Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological biodiversity studies. Nairobi, Kenya: World Agroforestry Centre (ICRAF).
48. Phillips S, Anderson R, Schapire R, (2006) Maximum entropy modeling of species geographic distributions. Ecological Modeling 190: 231-259.
49. Sankovski A, Barbour W, (2000) Pepper W, (2000) Quantification of the IS99 emission scenario storylines using the atmospheric stabilization framework (ASF). Technological Forecasting & Social Change 63: 263-287.
50. Liu C, Berry PM, Dawson TP, Pearson RG, (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28: 385-393.
51. Dickau R (2005) Resource use, crop dispersals, and the transition to agriculture in prehistoric Panama: evidence from starch grains and macroremains. PhD dissertation, Temple University.
52. Bartley GD (2005) The genetic diversity of cacao and its utilization. Wallingford, UK: CABI Publishing.
53. d'Horta FM, Cabanne GS, Meyer D, Miyaki CY, (2011) The genetic effects of Late Quaternary climatic changes over a tropical latitudinal gradient: diversification of an Atlantic Forest passerine. Molecular Ecology 20: 1923-1935.
54. Resende HC, Yotoko KSC, Delabie JHC, Costa MA, Campiolo S, et al. (2010) Pliocene and Pleistocene events shaping the genetic diversity within the central corridor of the Brazilian Atlantic Forest. Biological Journal of the Linnean Society 101: 949-960.
55. Solomon SE, Bacci M, Martins J, Vinha GG, Mueller UG, (2008) Paleodistributions and comparative molecular phylogeography of leafcutter ants (Atta spp.) provide new insight into the origins of Amazonian diversity. PloS ONE 3: e2738.
56. Cheesman E, (1944) Notes on the nomenclature, classification and possible relationships of cocoa populations. Tropical Agriculture 21: 144-159.
57. Loor RG, Fouet O, Lemainque A, Pavek S, Risterucci A-M, et al. (2012) Origin and domestication of the Nacional cacao variety from Ecuador and collecting expedition of new related genetic resources. Plant and Animal Genome XX Conference (January 14-18, 2012).
58. Almeida CMVC de, Almeida CFG de, (1987) Coleta de cacau silvestre no Estado de Rondônia, Brasil. Revista Theobroma 17: 65-92.
59. Frankel OH, Brown AHD, Burdon J (1995b) The conservation of cultivated plants. In: The conservation of plant biodiversity. Cambridge, Great Britain: Cambridge University Press. 79-117.
60. Laurent V, Risterucci AM, Lanaud C, (1994) Genetic diversity in cocoa revealed by cDNA probes. Theoretical and Applied Genetics 88: 193-198.
61. Schroth G, Faria D, Araujo M, Bede L, Bael S, et al. (2011) Conservation in tropical landscape mosaics: the case of the cacao landscape of southern Bahia, Brazil. Biodiversity and Conservation 20: 1635-1654.
62. Fuller DQ, van Etten J, Manning K, Castillo C, Kingwell-Banham E, et al. (2011) The contribution of rice agriculture and livestock pastoralism to prehistoric methane levels: An archaeological assessment. The Holocene 21: 743-759.