Spatial structure and genetic diversity of natural populations of the Caribbean pine, Pinus caribaea var. bahamensis (Pinaceae), in the Bahaman archipelago

Botanical Journal of the Linnean Society

Volumn 174, Issue 3, 2014, Pages 359-383

  Sanchez, Michele ^a   Ingrouille, Martin J ^b   Cowan, Robyn S ^a   Hamilton, Martin A ^c   Fay, Michael F ^a  

^a JODRELL LABORATORY   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c ROYAL BOTANIC GARDENS   (United Kingdom)

Author keywords

Conservation genetics; Logging; Pine forests; Population genetics; Scale insects; Turks and Caicos; West Indies

Indexed keywords

CONIFEROUS TREE; FOREST MANAGEMENT; GENE FLOW; GENETIC DIFFERENTIATION; GENETIC MARKER; PLASTID; POPULATION STRUCTURE; RECOMBINATION; SPATIAL ANALYSIS; TAXONOMY;

TURKS AND CAICOS ISLANDS;

HEMIPTERA; PINACEAE; PINUS CARIBAEA; PINUS CARIBAEA VAR. BAHAMENSIS;

EID: 84894464640     PISSN: 00244074     EISSN: 10958339     Source Type: Journal    
DOI: 10.1111/boj.12146     Document Type: Article

References (135)

1. Anadón-Irizarry V, Wege DC, Upgren A, Young R, Boom B, León YM, Arias Y, Koenig K, Morales AL, Burke W, Pérez-Leroux A, Levy C, Koenig S, Gape L, Moore P. 2012. Sites for priority biodiversity conservation in the Caribbean Islands Biodiversity Hotspot. Journal of Threatened Taxa 4: 2806-2844.
2. André C, Larsson LC, Laikre L, Bekkevold D, Brigham J, Carvalho GR, Dahlgren TG, Hutchinson WF, Mariani S, Mudde K, Ruzzante DE, Ryman N. 2011. Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs. putatively selected loci. Heredity 106: 270-280.
3. Angeles ME, González JE, Erickson DJ, Hernández J. 2006. An assessment of future Caribbean climate changes using the BAU scenario by coupling a global circulation model with a regional model. XVIII Conference on Climate Variability and Change. Atlanta, GA: American Metereological Society.
4. Areces-Mallea AE, Weakley AS, Li X, Sayre RG, Parrish JD, Tipton CV, Boucher T. 1999. A guide to Caribbean vegetation types: preliminary classification system and descriptions. Arlington, VA: The Nature Conservancy.
5. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48.
6. Barbará T, Martinelli G, Fay MF, Mayo SJ, Lexer C. 2007. Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude 'inselbergs', Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Molecular Ecology 16: 1981-1992.
7. Barrett WH, Golfari L. 1962. Descripción de dos nuevas variedades del 'pino del Caribe' (Pinus caribaea Mor.). Caribbean Forester 23: 59-71.
8. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. 1996-2004. GENETIX 4.05, Windows TM software for population genetics. Montpellier: Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II.
9. Blick JP. 2007. Pre-Columbian impact on terrestrial, intertidal, and marine resources, San Salvador, Bahamas (A.D. 950-1500). Journal for Nature Conservation 15: 174-183.
10. Bounds JH. 1981. Land use on New Providence Island, Bahamas 1960-1979. Revista Geográfica 94: 123-153.
11. Brook BW. 2008. Demographics versus genetics in conservation biology. In: Carroll SP, Fox CW, eds. Conservation biology: evolution in action. New York: Oxford University Press, 35-49.
12. Bucci G, González-Martínez SC, Le Provost G, Plomion C, Ribeiro MM, Sebastiani F, Alia R, Vendramin GG. 2007. Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Molecular Ecology 16: 2137-2153.
13. Burke JM, Tang S, Knapp SJ, Rieseberg LH. 2002. Genetic analysis of sunflower domestication. Genetics 161: 1257-1267.
14. Caballero A, Toro MA. 2002. Analysis of genetic diversity for the management of conserved subdivided populations. Conservation Genetics 3: 289-299.
15. Clark CM, Wentworth TR, O'Malley DM. 2000. Genetic discontinuity revealed by chloroplast microsatellites in eastern North American Abies (Pinaceae). American Journal of Botany 87: 774-782.
16. Clark JM. 1988. Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Research 16: 9677-9686.
17. Clerveaux W, Fisher T. 2006. Part I - case study: Turks and Caicos Islands. In: Tietze U, Haughton M, Siar SV, eds. Socio-economic indicators in integrated coastal zone and community-based fisheries management. Case studies from the Caribbean. Rome: FAO Fisheries, 125-139.
18. Coombs JA, Letcher BH, Nislow KH. 2008. CREATE: a software to create input files from diploid genotypic data for 52 genetic software programs. Molecular Ecology Resources 8: 578-580.
19. De Lucas AI, Robledo-Arnuncio JJ, Hidalgo E, González-Martínez SC. 2008. Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 100: 390-399.
20. Delgado P, Piñero D, Rebolledo V, Jardón L, Chi F. 2011. Genetic variation and demographic contraction of the remnant populations of Mexican Caribbean pine (Pinus caribaea var. hondurensis: Pinaceae). Annals of Forest Science 68: 121-128.
21. DeWoody J, Nason JD, Hipkins VD. 2006. Mitigating scoring errors in microsatellite data from wild populations. Molecular Ecology Notes 6: 951-957.
22. Doran E Jr. 1958. The Caicos conch trade. Geographical Review 48: 388-401.
23. Doyle JH, Verhoeven RL, Bester C, Wingfield BD, Botha AM. 2002. Germ-furrow morphology and storage conditions determine the degree of viability of Pinus caribaea pollen. South African Journal of Botany 68: 457-463.
24. Doyle JJ, Dickson EE. 1987. Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36: 715-722.
25. Dvorak WS, Hamrick JL, Gutierrez EA. 2005. The origin of Caribbean pine in the seasonal swamps of the Yucatán. International Journal of Plant Science 166: 985-994.
26. Dvorak WS, Jordon AP, Hodge GP, Romero JL. 2000. Assessing evolutionary relationships of pines in the Oocarpae and Australes subsections using RAPD markers. New Forests 20: 163-192.
27. Dzialuk A, Boratyński A, Boratyńska K, Burczyk J. 2012. Geographic patterns of genetic diversity of Pinus mugo (Pinaceae) in Central European mountains. Dendrobiology 68: 31-41.
28. Echt CS, DeVerno LL, Anzidei M, Vendramin GG. 1998. Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Molecular Ecology 7: 307-316.
29. Elsik CG, Minihan VT, Hall SE, Scarpa AM, Williams CG. 2000. Low-copy microsatellite markers for Pinus taeda L. Genome 43: 550-555.
30. Excoffier L, Heckel G. 2006. Computer programs for population genetics data analysis: a survival guide. Nature Reviews Genetics 7: 745-758.
31. Excoffier L, Laval G, Schneider S. 2005. ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
32. 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.
33. Farjon A, De la Rosa JAP, Styles BT. 1997. A field guide to the pines of Mexico and Central America. Kew: Royal Botanic Gardens.
34. Farjon A, Page CN. 2003. Diversity in strategies for conifer conservation, the action plan and future developments. In: Mill RR, ed. Proceedings of the IV International Conifer Conference. Wye College, UK: Acta Horticulturae (ISHS), 397-403.
35. Farjon A, Styles BT. 1997. Monograph 75. Pinus (Pinaceae). Flora Neotropica. New York: New York Botanical Garden Press on behalf of Organization for Flora Neotropica.
36. Fernando D, Lazzaro M, Owens J. 2005. Growth and development of conifer pollen tubes. Sexual Plant Reproduction 18: 149-162.
37. Fisher PJ, Richardson TE, Gardner RC. 1998. Characteristics of single- and multi-copy microsatellites from Pinus radiata. Theoretical and Applied Genetics 96: 969-979.
38. Flint-García SA, Thornsberry JM, Buckler ES IV. 2003. Structure of linkage disequilibrium in plants. Annual Review of Plant Biology 54: 357-374.
39. Frankham R. 1996. Relationship of genetic variation to population size in wildlife. Conservation Biology 10: 1500-1508.
40. Frankham R. 2005. Genetics and extinction. Biological Conservation 126: 131-140.
41. Frankham R. 2010. Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143: 1919-1927.
42. Fu YX. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
43. Godbout J, Beaulieu J, Bousquet J. 2010. Phylogeographic structure of jack pine (Pinus banksiana; Pinaceae) supports the existence of a coastal glacial refugium in northeastern North America. American Journal of Botany 97: 1903-1912.
44. González-Martínez SC, Burczyk J, Nathan RA, Nanos N, Gil L, Alia R. 2006. Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Molecular Ecology 15: 4577-4588.
45. Goudet J. 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485-486.
46. Greaves A. 1978. Description of seed sources and collections for provenances of Pinus caribaea. Oxford: Department of Forestry, Commonwealth Forestry Institute, University of Oxford.
47. Guillot G, Estoup A, Mortier F, Cosson JF. 2005a. A spatial statistical model for landscape genetics. Genetics 170: 1261-1280.
48. Guillot G, Mortier F, Estoup A. 2005b. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5: 712-715.
49. Guo SW, Thompson EA. 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361-372.
50. Gupta PK, Rustgi S, Kulwal PL. 2005. Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Molecular Biology 57: 461-485.
51. Henry PWT. 1974. The pine forests of the Bahamas. Surbiton: Land Resources Division.
52. Hollingsworth PM, Ennos RA. 2004. Neighbour joining trees, dominant markers and population genetic structure. Heredity 92: 490-498.
53. Jaramillo-Correa JP, Aguirre-Planter E, Khasa DP, Eguiarte LE, Pinero D, Furnier GR, Bousquet J. 2008. Ancestry and divergence of subtropical montane forest isolates: molecular biogeography of the genus Abies (Pinaceae) in southern Mexico and Guatemala. Molecular Ecology 17: 2476-2490.
54. Jardón-Barbolla L, Delgado-Valerio P, Geada-López G, Vázquez-Lobo A, Piñero D. 2011. Phylogeography of Pinus subsection Australes in the Caribbean basin. Annals of Botany 107: 229-241.
55. Kairo M, Ali B, Cheeseman O, Haysom K, Murphy S. 2003. Invasive species threats in the Caribbean region: report to the Nature Conservancy. Wallingford: CAB International.
56. Kalinowski ST. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5: 539-543.
57. Kellogg RS. 1951. Yellow pine in the Bahamas. Journal of Forestry 49: 795-796.
58. Kettle CJ, Ennos RA, Jaffré T, McCoy S, Le Borgne T, Gardner M, Hollingsworth PM. 2011. Importance of demography and dispersal for the resilience and restoration of a critically endangered tropical conifer Araucaria nemorosa. Diversity and Distributions 18: 248-259.
59. Kjellmark E. 1996. Late Holocene climate change and human disturbance on Andros Island, Bahamas. Journal of Paleolimnology 15: 133-145.
60. Kramer AT, Havens K. 2009. Plant conservation genetics in a changing world. Trends in Plant Science 14: 599-607.
61. Kramer AT, Ison JL, Ashley MV, Howe HF. 2008. The paradox of forest fragmentation genetics. Conservation Biology 22: 878-885.
62. Kutil BL, Williams CG. 2001. Triplet-repeat microsatellites shared among hard and soft pines. Heredity 92: 327-332.
63. Leberg PL. 2002. Estimating allelic richness: effects of sample size and bottlenecks. Molecular Ecology 11: 2445-2449.
64. Ledig FT. 1998. Genetic variation in pines. In: Richardson DM, ed. Ecology and biogeography of Pinus. Cambridge: Cambridge University Press, 251-280.
65. Ledig FT, Capo-Arteaga MA, Hodgskiss PD, Sbay H, Flores-López C, Conkle MT, Bermejo-Velazquez B. 2001. Genetic diversity and the mating system of a rare Mexican piñon, Pinus pinceana, and a comparison with Pinus maximartinezii (Pinaceae). American Journal of Botany 88: 1977-1987.
66. Levene H. 1949. On a matching problem arising in genetics. The Annals of Mathematical Statistics 20: 91-94.
67. Little JEL, Dorman KW. 1954. Slash pine (Pinus elliottii) including South Florida slash pine nomenclature and description. Asheville, NC: Department of Agriculture, Forest Service, Southeastern Forest Experiment Station.
68. Malumphy C, Hamilton MA, Manco BN, Green PWC, Sanchez MD, Corcoran M, Salamanca E. 2012. Toumeyella parvicornis (Hemiptera: Coccidae), causing severe decline of Pinus caribaea var. bahamensis in the Turks and Caicos Islands. Florida Entomologist 95: 113-119.
69. March EW. 1949. Pine forests of the Bahamas. Empire Forestry Research 28: 33-37.
70. Mariette S, Chagne D, Lezier C, Pastuszka P, Raffin A, Plomion C, Kremer A. 2001. Genetic diversity within and among Pinus pinaster populations: comparison between AFLP and microsatellite markers. Heredity 86: 469-479.
71. Maunder M, Leiva A, Santiago-Valentín E, Stevenson DW, Acevedo-Rodríguez P, Meerow AW, Mejía M, Clubbe C, Francisco-Ortega J. 2008. Plant conservation in the Caribbean island biodiversity hotspot. The Botanical Review 74: 197-207.
72. Meirmans PG. 2006. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60: 2399-2402.
73. Miller W. 1920. Forests in the colony of the Bahamas. British Empire Forestry Conference. London: His Majesty's Stationery Office.
74. Moritz C. 1994. Defining evolutionarily significant units for conservation: 100th issue essays. Trends in Ecology & Evolution 9: 373-375.
75. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
76. Mylroie JE. 2008. Late Quaternary sea-level position: evidence from Bahamian carbonate deposition and dissolution cycles. Quaternary International 183: 61-75.
77. Nathan R, Safriel UN, Noy-Meir I, Schiller G. 2000. Spatiotemporal variation in seed dispersal and recruitment near and far from Pinus halepensis trees. Ecology 81: 2156-2169.
78. Navascués M, Emerson BC. 2005. Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Molecular Ecology 14: 1333-1341.
79. Nei M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 70: 3321-3323.
80. Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
81. Nei M, Chesser RK. 1983. Estimation of fixation indices and gene diversities. Annals of Human Genetics 47: 253-259.
82. Nelson CD, Josserand S, Echt CS, Koppelman J. 2007. Loblolly pine SSR markers for shortleaf pine genetics. In: Kabrick JM, Dey DC, Gwaze D, eds. Shortleaf pine restoration and ecology in the Ozarks: proceedings of a symposium. Springfield: General Technical Report NRS-P-15. Newton Square, PA: US Department of Agriculture, Forest Service, Northern Research Station, 95-98.
83. Nelson CD, Nance WL. 1994. Chloroplast DNA variation among and within taxonomic varieties of Pinus caribaea and Pinus elliottii. Canadian Journal of Forest Research 24: 424-426.
84. Palma-Silva C, Cavallari MM, Barbará T, Lexer C, Gimenes MA, Bered F, Bodanese-Zanettini MH. 2007. A set of polymorphic microsatellite loci for Vriesea gigantea and Alcantarea imperialis (Bromeliaceae) and cross-amplification in other bromeliad species. Molecular Ecology Notes 7: 654-657.
85. Peakall R, Smouse PE. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295.
86. Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG. 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14: 689-701.
87. Petit RJ, el Mousadik A, Pons O. 1998. Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12: 844-855.
88. Powell W, Morgante M, McDevitt R, Vendramin GG, Rafalski JA. 1995. Polymorphic simple sequence repeat regions in chloroplast genomes: applications to the population genetics of pines. Proceedings of the National Academy of Sciences of the United States of America 92: 7759-7763.
89. Provan J, Powell W, Hollingsworth PM. 2001. Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends in Ecology and Evolution 16: 142-147.
90. Radabaugh BE. 1974. Kirtland's warbler and its Bahama wintering grounds. The Wilson Bulletin 86: 374-383.
91. Rajora OP, DeVerno L, Mosseler A, Innes DJ. 1998. Genetic diversity and population structure of disjunct Newfoundland and central Ontario populations of eastern white pine (Pinus strobus). Canadian Journal of Botany 76: 500-508.
92. Reid SB. 2010. The complex architecture of New Providence Island (Bahamas) built during the Pleistocene sea level highstands. Unpublished M.Sc. Thesis, University of Miami.
93. Richardson JE, Fay MF, Cronk QC, Chase MW. 2003. Species delimitation and the origin of populations in island representatives of Phylica (Rhamnaceae). Evolution 57: 816-827.
94. Robbins AMJ, Eckelmann CM, Quiñones M. 2010. Forest fires in the Insular Caribbean. AMBIO: A Journal of the Human Environment 37: 528-534.
95. Robledo-Arnuncio JJ, Collada C, Alía R, Gil L. 2005. Genetic structure of montane isolates of Pinus sylvestris L. in a Mediterranean refugial area. Journal of Biogeography 32: 595-605.
96. Rousset F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219-1228.
97. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW. 1984. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proceedings of the National Academy of Sciences of the United States of America 81: 8014-8018.
98. Sanchez M. 2012. Conservation genetics and biogeography of the Caribbean pine (Pinus caribaea var. bahamensis) in the Bahaman archipelago. Unpublished D.Phil. Thesis, Birkbeck University of London.
99. Sanchez M, Hamilton MA, Farjon A. 2013. Pinus caribaea var. bahamensis. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. Available at: http://www.iucnredlist.org Downloaded on 21 August 2013.
100. Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA. 1998. Phylogeographic studies in plants: problems and prospects. Molecular Ecology 7: 465-474.
101. Schuelke M. 2000. An economic method for the fluorescent labelling of PCR fragments - a poor man's approach to genotyping for research and high-throughput diagnostics. Nature Biotechnology 18: 233-234.
102. Sealey NE. 1985. Bahamian landscapes - an introduction to the geography of the Bahamas. London: Collins Caribbean.
103. Selkoe KA, Toonen RJ. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9: 615-629.
104. Shea KL, Furnier GR. 2002. Genetic variation and population structure in central and isolated populations of balsam fir, Abies balsamea (Pinaceae). American Journal of Botany 89: 783-791.
105. Shepherd M, Cross M, Dieters MJ, Henry R. 2003. Genetic maps for Pinus elliottii var. elliottii and P. caribaea var. hondurensis using AFLP and microsatellite markers. Theoretical and Applied Genetics 106: 1409-1419.
106. Shepherd M, Cross M, Maguire TL, Dieters MJ, Williams CG, Henry RJ. 2002. Transpecific microsatellites for hard pines. Theoretical and Applied Genetics 104: 819-827.
107. Shepherd M, Williams CG. 2008. Comparative mapping among subsection Australes (genus Pinus, family Pinaceae). Genome 51: 320-331.
108. Slatkin M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787-792.
109. Slatkin M. 1993. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264-279.
110. Slatkin M. 1994. Linkage disequilibrium in growing and stable populations. Genetics 137: 331-336.
111. Smouse PE, Long JC. 1992. Matrix correlation analysis in anthropology and genetics. American Journal of Physical Anthropology 35: 187-213.
112. Smouse PE, Long JC, Sokal RR. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Biology 35: 627-632.
113. Steadman DW, Franz R, Morgan GS, Albury NA, Kakuk B, Broad K, Franz SE, Tinker K, Pateman MP, Lott TA, Jarzen DM, Dilcher DL. 2007. Exceptionally well preserved late Quaternary plant and vertebrate fossils from a blue hole on Abaco, The Bahamas. Proceedings of the National Academy of Sciences of the United States of America 104: 19897-19902.
114. Stone LHJ. 1953. The weather of the Bahamas. Weather 8: 301-302.
115. The Commonwealth of the Bahamas. 2005. National policy for the adaptation to climate change. In: The National Climate Change Committee, BEST, ed. Nassau: The Bahamas Environment, Science & Technology Commission - BEST.
116. The Commonwealth of the Bahamas. 2008. The 2000 census of population and housing report - all Bahamas. Nassau: Department of Statistics of the Bahamas.
117. The Turks and Caicos Islands. 2001. TCI census atlas. Grand Turk, TCI: Statistical Office, Department of Economic Planning and Statistics.
118. Tushingham AM, Peltier WR. 1991. Ice-3G: a new global model of Late Pleistocene deglaciation based upon geophysical predictions of post-glacial relative sea level change. Journal of Geophysical Research 96: 4497-4523.
119. Van Oosterhout C, Hutchinson F, Wills DPM, Shipley P. 2004. MICRO_CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538.
120. Van Zonneveld M, Jarvis A, Dvorak W, Lema G, Leibing C. 2009. Climate change impact predictions on Pinus patula and Pinus tecunumanii populations in Mexico and Central America. Forest Ecology and Management 257: 1566-1576.
121. Vendramin GG, Fady B, González-Martínez SC, Hu FS, Scotti I, Sebastiani F, Soto A, Petit RJ. 2008. Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution 62: 680-688.
122. Vendramin GG, Lelli L, Rossi P, Morgante M. 1996. A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Molecular Ecology 5: 595-598.
123. Vendramin GG, Ziegenhagen B. 1997. Characterisation and inheritance of polymorphic plastid microsatellites in Abies. Genome 40: 857-864.
124. Weir BS. 1996. Genetic data analysis II: methods for discrete population genetic data. Sunderland, MA: Sinauer Associates.
125. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
126. Whitaker FF, Smart PL. 1997. Hydrogeology of the Bahamian archipelago. In: Vacher HL, Quinn T, eds. Geology and hydrogeology of carbonate islands. Developments in sedimentology No. 54. Amsterdam: Elsevier Science B.V., 183-216.
127. Williams CG. 2008. Aerobiology of Pinus taeda pollen clouds. Canadian Journal of Forest Research 38: 2177-2188.
128. Williams CG. 2010. Long-distance pine pollen still germinates after meso-scale dispersal. American Journal of Botany 97: 846-855.
129. Williams DA, Wang Y, Borchetta M, Gaines MS. 2007. Genetic diversity and spatial structure of a keystone species in fragmented pine rockland habitat. Biological Conservation 138: 256-268.
130. Williams JW, Shuman BN, Thompson III W, Bartlein PJ, Leduc PL. 2004. Late-Quaternary vegetation dynamics in North America: scaling from taxa to biomes. Ecological Monographs 74: 309-334.
131. Wolfe KH, Li WH, Sharp PM. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America 84: 9054-9058.
132. Wright S. 1943. Isolation by distance. Genetics 28: 114-138.
133. Wright S. 1951. The genetical structure of populations. Annals of Human Genetics 15: 323-354.
134. Wright S. 1965. The interpretation of population structure by F-statistics with special regards to systems of mating. Evolution 19: 395-420.
135. Zheng YQ, Ennos RA. 1999. Genetic variability and structure of natural and domesticated populations of Caribbean pine (Pinus caribaea Morelet). Theoretical and Applied Genetics 98: 765-771.