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Genetic diversity and gene flow in a Caribbean tree Pterocarpus officinalis Jacq.: a study based on chloroplast and nuclear microsatellites

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Abstract

We analysed the molecular diversity of Pterocarpus officinalis, a tree species distributed in Caribbean islands, South and Central America to quantify the genetic variation within island, to assess the pattern of differentiation and infer levels of gene flow; with the overall goal of defining a strategy of conservation. Two hundred two individuals of 9 populations were analysed using three chloroplast and six nuclear microsatellite markers. The observed heterozygosity varied markedly among the populations for nuclear (H Onuc = 0.20–0.50) and chloroplast microsatellites (H cp = 0.22–0.68). The continental population from French Guyana showed a higher value of H Onuc than island populations, and the differences were significant in some cases. The fixation index F IS ranged from −0.043 to 0.368; a significant heterozygote deficit was detected in 7 populations. The heterozygosity excess method suggested that two populations in Guadeloupe have undergone a recent bottleneck. Global and pairwise F ST were high for both nuclear (F STnuc = 0.29) and chloroplast microsatellites (F STcp = 0.58). The neighbour-joining tree based on both markers, presented a differentiation pattern that can be explained by the seed dispersal by flotation and marine stream. The comparison of Bayesian approach and the method based on allelic frequency demonstrate a very limited number of migrants between populations.

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References

  • Aldrich PR, Hamrick JL, Chavarriaga P, Kochert G (1998) Microsatellite analysis of demographic genetic structure in fragmented populations of the tropical tree Symphonia globulifera. Mol Ecol 7:933–944

    Article  PubMed  CAS  Google Scholar 

  • Andrianoelina O, Rakotondraoelina H, Ramamonjisoa L, Danthu P, Bouvet J-M (2005) Genetic diversity of Dalbergia monticola (Fabaceae), an endangered tree species in the fragmented oriental forest of Madagascar. Biodivers Conserv 15:1109–1128

    Article  Google Scholar 

  • Bacon (1990) Ecology and management swamp forest in the Guianas and Caribbean region. Ecosyst World 15:213–250

  • Baldoni L, Tosti N, Ricciolini C, Belaj A, Arcioni S, Pannelli G, Germana M A, Mulas M, Porceddu A (2006) Genetic structure of wild and cultivated olives in the Central Mediterranean basin. Ann Bot 98:935–942

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH (1996) The reproductive biology and genetics of island plants. Philos Trans R Soc Lond Ser B 351:725–733

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) GENETIX 4.03. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier, France. http://www.univ-montp2.fr/~genetix/genetix/genetix.htm

  • Bottin L, Verhaegen D, Tassin J, Vaillant A, Bouvet J-M (2005) Genetic diversity and population structure of an insular tree, Santalum austrocaledonicum in New Caledonian archipelago. Mol Ecol 14:1979-1989

    Article  PubMed  CAS  Google Scholar 

  • Bottin L, Tassin J, Nasi R, Bouvet J-M (2007) Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia. Conserv Genet 8:99–109

    Article  Google Scholar 

  • Bousquet J, Simon L, Lalonde M (1990) DNA amplification from vegetative and sexual tissues of trees using polymerase chain reaction. Can J For Res 20:254–257

    Article  CAS  Google Scholar 

  • Bryan GJ, McNicoll J, Ramsay G, Meyer RC, De Jong WS (1999) Polymorphic simple sequence repeat markers in chloroplast genomes of solanaceous plants. Theor Appl Genet 99:859–867

    Article  CAS  Google Scholar 

  • Butaud (2006) Contribution à la connaissance d’un arbre insulaire en voie de disparition, le santal de Polynésie française (Santalum insulare): Etudes écologiques, morphologiuques, génétique et chimiques. Ph D dissertation. University of French Polynesia

  • Butaud JF, Rives F, Verhaegen D, Bouvet J-M, (2005) Phylogeography of Eastern Polynesian sandalwood (Santalum insulare), an endangered tree species from the Pacific: a study based on chloroplast microsatellites. J Biogeogr 32:1763–1774

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Gen 19:233–257

    CAS  Google Scholar 

  • Cintrón BB (1983) Coastal freshwater swamp forests: Puerto Rico’s most endangered ecosystem. A. E. Lugo Los bosques de Puerto Rico. Institute of Tropical Forestry, USDA Forest Service, Rio Piedras P.R, pp 249–282

  • Collevatti RG, Grattapaglia D, Hay JD (2001) Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Mol Ecol 10:349–356

    Article  PubMed  CAS  Google Scholar 

  • Collevatti RG, Grattapaglia D, Hay JD (2003) Evidence for multiple lineages of Caryocar brasiliense populations in the Brazilian Cerrado based on the analysis of chloroplast DNA sequence and microsatellite haplotype variation. Mol Ecol 12:105–115

    Article  PubMed  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Dutech C, Joly HI, Jarne 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

    Article  PubMed  CAS  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • England PR, Usher AV, Whelan RJ, Ayre DJ (2002) Microsatellite diversity and genetic structure of fragmented populations of the rare, fire-dependent shrub Grevillea macleayana. Mol Ecol 11:967–977

    Article  PubMed  CAS  Google Scholar 

  • Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2007) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP: Phylogenetic inference package, version 6.1. University of Washington, Seattle, WA, USA

    Google Scholar 

  • Fontaine C, Lovett PN, Sanou H, Maley J, Bouvet J-M (2004) Genetic diversity of the shea tree (Vitellaria paradoxa C.F. Gaertn.), detected by RAPD and chloroplast microsatellite markers. Heredity 93:639–648

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:500–1508

    Article  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Gomez A, Gonzalez-Martinez SC, Collada C, Climent J, Gill L (2003) Complex population genetic structure in the endemic Canary Island pine revealed using chloroplast microsatellite markers. Theor Appl Genet 107:1123–1131

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3) http://www.nil.ch/izea/softwares/fstat.html

  • Graham A (1995) Diversification of Gulf/Caribbean mangrove communities through Cenozoic time. Biotropica 27:20–27

    Article  Google Scholar 

  • Grivet D, Petit RJ (2003) Chloroplast DNA phylogeography of the hornbeam in Europe: evidence for a bottleneck at the outset of postglacial colonization. Conserv Gen 4:47–56

    Article  CAS  Google Scholar 

  • Hamilton MH, Miller JR (2002) Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure. Genetics 162:1897–1909

    PubMed  Google Scholar 

  • Henry JP (1999): Précis de génétique des populations: cours, exercices et problèmes résolus (Sciences Sup) 186 pp

  • Hurlbert SH (1971) The non-concept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • Imbert D, Bland F, Russier F (1988) Les milieux humides du littoral guadeloupéen. Office national des forêts 40–49

  • Imbert D, Bonheme I, Saur E, Bouchon C (2000) Floristics and structure of Pterocarpus officinalis swamp forest in Guadeloupe, Lesser Antilles. J Trop Ecol 16:55–68

    Article  Google Scholar 

  • 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 12:2845–2883

    Article  Google Scholar 

  • Lhuillier E, Butaud J-F, Bouvet J-M (2006) Extensive clonality and strong differentiation in the insular Pacific tree Santalum insulaire: implications for its conservation. Ann Bot 98:1061–1072

    Article  PubMed  CAS  Google Scholar 

  • Little EL, Wadsworth FH (1964) Common trees of Puerto Rico and the Virgin Islands. Forest Service, US Dept. of Agriculture, Washington, DC. Agricultural Handbook No. 249, 1217 pp

  • Lopez OR (2001) Seed flotation and post-flooding germination in tropical terra firma and seasonally flooded forest species. Funct Ecol 15:763–771

    Article  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recent bottleneck populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Mank JE, Avise JC (2004) Individual organisms as units of analysis: Bayesian-clustering alternatives in population genetics. Genet Res Camb 84:135–143

    CAS  Google Scholar 

  • Marshall HD, Newton C, Ritland K (2002) Chloroplast phylogeography and evolution of highly polymorphic microsatellites in lodgepole pine (Pinus contorta). Theor Appl Genet 104:367–378

    Article  CAS  Google Scholar 

  • Moritz C (1994) Defining significant units for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Muller F, Vaillant A, Bâ A, Bouvet J-M (2005) Isolation and Characterization of microsatellite markers in Pterocarpus officinalis Jacq. Mol Ecol Notes 6:462–464

    Article  Google Scholar 

  • Navascués M, Emerson BC (2005) Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Mol Ecol 14:1333–1341

    Article  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY, USA

    Google Scholar 

  • Novick RR, Dick CD, Lemes MR, Navarro C, Caccon A, Bermingham E (2003) Genetic structure of Mesoamerican population of big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Mol Ecol 12:2885–2893

    Article  PubMed  Google Scholar 

  • Parks JC, Werth CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). Am J Bot 80:537–544

    Article  Google Scholar 

  • Palme AE, Vendramin GG (2002) Chloroplast DNA variation, postglacial recolonization and hybridization in hazel, Corylus avellana. Mol Ecol 11:1769–1779

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in effective population size from allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen W (2004) Documentation for structure 2.0β. Available at: http://pritch.bsd.uchicago.edu

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rivera-Ocasio E, Aide TM, McMillan W (2002) Patterns of genetic diversity and biogeographical history of the tropical wetland tree, Pterocarpus officinalis (Jacq.), in the Caribbean basin. Mol Ecol 11:675–683

    Article  PubMed  CAS  Google Scholar 

  • Rossetto M, Slade RW, Baverstock PR, Henry RJ, Lee LS (1999) Microsatellite variation and assessment of genetic structure in tea tree (Melaleuca alternifolia – Myrtaceae). Mol Ecol 8:633–643

    Article  PubMed  CAS  Google Scholar 

  • Rousset F (1996) Genetic differentiation and estimation of gene flow from F-statitics under isolation by distance. Genetics 145:1219–1228

    Google Scholar 

  • Sanou H, Lovett N, Bouvet J-M (2005) Comparison of quantitative and molecular variation in agroforestry populations of the shea tree (Vitellaria paradoxa C.F. Gaertn) in Mali. Mol Ecol 14:2601–2610

    Article  PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2000: a software for population genetics data analysis. Genetics and Biometrics Laboratory, Department of Anthropology, University of Geneva, Geneva, Switzerland

    Google Scholar 

  • Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43:1349–1368

    Article  Google Scholar 

  • Stenberg P, Lundmark M, Saura A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes 3:329–331

    Article  CAS  Google Scholar 

  • Storfer A. (1996) Quantitative genetics: a promising approach for the assessment of genetic variation in endangered species. Trends Ecol Evol 11:343–348

    Article  Google Scholar 

  • Tapio M, Miceikiene I, Vilkki J, Kantanen J (2003) Comparison of microsatellite and blood protein diversity in sheep: inconsistencies in fragmented breeds. Mol Ecol 12:2045–2056

    Article  PubMed  CAS  Google Scholar 

  • Tani N ,Yoshimaru H, Kawahara T, Hoshi Y, Nobushima F, Yasui T (2006) Determination of the genetic structure of remnant Morus boninensis Koidz. trees to establish a conservation program on the Bonin Islands, Japan. BMC Ecol 6:14. doi:10.1186/1472-6785-6-14

  • Tassin J (1999) Plant invaders in Réunion Island (French Overseas Territory, Indian Ocean). Aliens 9:10

    Google Scholar 

  • Tsuda Y, Ide Y (2005) Wide-range analysis of genetic structure of Betula maximowicziana, a long-lived pioneer tree species and noble hardwood in the cool temperate zone of Japan. Mol Ecol 14:3929–3941

    Article  PubMed  CAS  Google Scholar 

  • Wang J (2004) Application of one-migrant-per-generation rule to conservation and management. Conserv Biol 18:332–343

    Article  Google Scholar 

  • Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    Article  PubMed  CAS  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST  ≠  1/(4Nm + 1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the French Ministry MEDD (Ministère de L’Ecologie et du Développement Durable) for financial support in implementing the Pterocarpus officinalis project. This work was supported financially by the Guadeloupe Archipelago Region and the Social European Fund. We are very grateful to colleagues at CIRAD, C. Leroux, G. Bena, and at the University of Antilles-Guyane for assistance in collecting samples, and to A. Vaillant and M. Poitel at CIRAD for their technical assistance in the laboratory. We are grateful to the two anonymous reviewers for their helpful comments and suggestions which improve significantly the manuscript.

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Authors and Affiliations

  1. Biological System Department, Research unit “genetic diversity and breeding of forest tree species”, CIRAD, Campus international de Baillarguet TA-A 39/C, 34398, Montpellier cedex 5, France

    F. Muller, M. Voccia & J. -M. Bouvet

  2. Laboratoire de Biologie et Physiologie Végétales, UFR des Sciences Exactes et Naturelles, Université des Antilles et de la Guyane, Campus Fouillole, BP. 592 97159, Pointe-a-Pitre, Guadeloupe, France

    F. Muller & A. Bâ

  3. Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR 1063 IRD/INRA/CIRAD/ENSA-M/UM2, Campus international de Baillarguet, TA 10/J, 34398, Montpellier cedex 5, France

    F. Muller

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  1. F. Muller
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Muller, F., Voccia, M., Bâ, A. et al. Genetic diversity and gene flow in a Caribbean tree Pterocarpus officinalis Jacq.: a study based on chloroplast and nuclear microsatellites. Genetica 135, 185–198 (2009). https://doi.org/10.1007/s10709-008-9268-4

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