Tropical Plant Biology

, Volume 1, Issue 1, pp 20–33 | Cite as

Spatial Scales of Pollen and Seed-Mediated Gene Flow in Tropical Rain Forest Trees

  • Christopher W. Dick
  • Olivier J. Hardy
  • F. Andrew Jones
  • Rémy J. Petit
Article

Abstract

Gene flow via seed and pollen is a primary determinant of genetic and species diversity in plant communities at different spatial scales. This paper reviews studies of gene flow and population genetic structure in tropical rain forest trees and places them in ecological and biogeographic context. Although much pollination is among nearest neighbors, an increasing number of genetic studies report pollination ranging from 0.5–14 km for canopy tree species, resulting in extensive breeding areas in disturbed and undisturbed rain forest. Direct genetic measures of seed dispersal are still rare; however, studies of fine scale spatial genetic structure (SGS) indicate that the bulk of effective seed dispersal occurs at local scales, and we found no difference in SGS (Sp statistic) between temperate (N = 24 species) and tropical forest trees (N = 15). Our analysis did find significantly higher genetic differentiation in tropical trees (FST = 0.177; N = 42) than in temperate forest trees (FST = 0.116; N = 82). This may be due to the fact that tropical trees experience low but significant rates of self-fertilization and bi-parental inbreeding, whereas half of the temperate tree species in our survey are wind pollinated and are more strictly allogamous. Genetic drift may also be more pronounced in tropical trees due to the low population densities of most species.

Keywords

Mating system Pollination Seed dispersal Spatial genetic structure Population differentiation 

Supplementary material

12042_2007_9006_MOESM1_ESM.xls (44 kb)
Supplemental material Table of published FST values for 82 temperate zone, 11 subtropical, and 42 tropical tree species. Also included, pollination mode (biotic or abiotic), stature of reproductive individuals (meters), type of marker used (allozyme, microsatellite, RAPD, AFLP, RFLP) (DOC 44 KB)

References

  1. 1.
    Aide TM (1986) The influence of wind and animal pollination on variation in outcrossing rates. Evolution 40(2):434–435Google Scholar
  2. 2.
    Aldrich PR, Hamrick JL (1998) Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281(5373):103–105PubMedGoogle Scholar
  3. 3.
    Alvarez-Buylla ER, Garcia-Barrios R, Lara-Moreno C, Martinez-Ramos M (1996) Demographic and genetic models in conservation biology: applications and perspectives for tropical rain forest tree species. Ann Rev Ecol Syst 27:387–421Google Scholar
  4. 4.
    Appanah S (1985) General flowering in the climax rain forest of Southeastern Asia. J Trop Ecol 1:225–240CrossRefGoogle Scholar
  5. 5.
    Apsit VJ, Hamrick JL, Nason JD (2001) Breeding population size of a fragmented population of a Costa Rican dry forest tree species. J Hered 92(5):415–420PubMedGoogle Scholar
  6. 6.
    Ashton PS (1969) Speciation among tropical forest trees: some deductions in the light of recent evidence. Biol J Linn Soc 1:155–196Google Scholar
  7. 7.
    Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae—new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132(1):44–66Google Scholar
  8. 8.
    Bacles CFE, Lowe AJ, Ennos RA (2006) Effective seed dispersal across a fragmented landscape. Science 311(5761):628–628PubMedGoogle Scholar
  9. 9.
    Baker HG (1959) Reproductive methods as factors in speciation in flowering plants. Cold Spr Harb Symp Quant Biol 24:177–199Google Scholar
  10. 10.
    Barrett SCH, Eckert CG (1990) Current issues in plant reproductive biology. Israel J Bot 39(1–2):5–12Google Scholar
  11. 11.
    Bawa KS (1990) Plant-pollinator interactions in tropical rainforests. Ann Rev Ecol Syst 21:399–422Google Scholar
  12. 12.
    Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution 29(1):167–179Google Scholar
  13. 13.
    Bawa KS, Opler PA (1977) Spatial relationships between staminate and pistillate plants of dioecious tropical forest trees. Evolution 31(1):64–68Google Scholar
  14. 14.
    Bawa KS, Perry DR, Beach JH (1985) Reproductive biology of tropical lowland rainforest trees. 1. sexual systems and incompatibility mechanisms. Am J Bot 72(3):331–345Google Scholar
  15. 15.
    Born C, Hardy OJ, Chevalier MH, Ossari S, Attéke EJW, Hossaert-Mckey M (2008) Small-scale spatial genetic structure in the central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Mol Ecol (in press) DOI 10.1111/j.1365-294X.2007.03685.x
  16. 16.
    Boshier DH, Chase MR, Bawa KS (1995) Population genetics of Cordia alliadora (Boraginaceae), a neotropical tree. 3. Gene flow, neighborhood, and population substructure. Am J Bot 82(4):484–490Google Scholar
  17. 17.
    Bullock SH (1994) Wind pollination of neotropical dioecious trees. Biotropica 26(2):172–179Google Scholar
  18. 18.
    Cascante A, Quesada M, Lobo JJ, Fuchs EA (2002) Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Consyt Biol 16(1):137–147Google Scholar
  19. 19.
    Chase MR, Moller C, Kesseli R, Bawa KS (1996) Distant gene flow in tropical trees. Nature 383(6599):398–399Google Scholar
  20. 20.
    Cloutier D, Hardy OJ, Caron H, Ciampi AY, Degen B, Kanashiro M, Schoen DJ (2007a) Low inbreeding and high pollen dispersal distances in populations of two Amazonian forest tree species. Biotropica 39(3):406–415Google Scholar
  21. 21.
    Cloutier D, Kanashiro M, Ciampi AY, Schoen DJ (2007b) Impact of selective logging on inbreeding and gene dispersal in an Amazonian tree population of Carapa guianensis Aubl. Mol Ecol 16(4):797–809PubMedGoogle Scholar
  22. 22.
    Collevatti RG, Grattapaglia D, Hay JD (2001) High resolution microsatellite based analysis of the mating system allows the detection of significant biparental inbreeding in Caryocar brasiliense, an endangered tropical tree species. Heredity 86:60–67PubMedGoogle Scholar
  23. 23.
    Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster RB, Itoh A, LaFrankie JV, Lee HS, Losos E, Manokara N, Sukumar R, Yamakura T (2000) Spatial patterns in the distribution of tropical tree species. Science 288:1414–1418PubMedGoogle Scholar
  24. 24.
    Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen, pp 298–313Google Scholar
  25. 25.
    Corner EJH (1954) The evolution of tropical forests. In: Huxley J, Hardy AC, Ford EC (eds) Evolution as a process. Allen and Unwin, London, pp 34–46Google Scholar
  26. 26.
    da Silva Carneiro F, Sebbenn AM, Kanashiro M, Degen B (2007) Low interannual variation of mating system and gene flow of Symphonia globulifera in the Brazilian Amazon. Biotropica 39(5):628–636Google Scholar
  27. 27.
    Dawson IK, Waugh R, Simons AJ, Powell W (1997) Simple-sequence repeats provide a direct estimate of pollen-mediated gene dispersal in the tropical tree Gliricidia sepium. Mol Ecol 6:179–183Google Scholar
  28. 28.
    Degen B, Bandou E, Caron H (2004) Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana. Heredity 93(6):585–591PubMedGoogle Scholar
  29. 29.
    Diamond JM, Gilpin ME, Mayr E (1976) Species-distance relation for birds of the Solomon archipelago, and the paradox of the great speciators. Proc Natl Acad Sci U S A 73:2160–2164PubMedGoogle Scholar
  30. 30.
    Dick CW (2001) Genetic Rescue of Remnant Tropical Trees by an Alien Pollinator. Proc Roy Soc Lond Ser B Biol Sci 268:2391–2396Google Scholar
  31. 31.
    Dick CW, Abdul-Salim K, Bermingham E (2003a) Molecular systematics reveals cryptic Tertiary diversification of a widespread tropical rainforest tree. Am Nat 162(12):691–703PubMedGoogle Scholar
  32. 32.
    Dick CW, Etchelecu G, Austerlitz F (2003b) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12(3):753–765PubMedGoogle Scholar
  33. 33.
    Dick CW, Bermingham E, Lemes MR, Gribel R (2007) Extreme long distance dispersal of the lowland rainforest tree Ceiba pentandra L. (Malvaceae) in Africa and the Neotropics. Mol Ecol 16:3039–3049PubMedGoogle Scholar
  34. 34.
    Doligez A, Joly HI (1997a) Genetic diversity and spatial structure within a natural stand of a tropical forest tree species, Carapa procera (Meliaceae), in French Guiana. Heredity 79:72–82Google Scholar
  35. 35.
    Doligez A, Joly HI (1997b) Mating system of Carapa procera (Meliaceae) in the French Guiana tropical forest. Am J Bot 84(4):461–70Google Scholar
  36. 36.
    Dunphy BK, Hamrick JL, Schwagerl J (2004) A comparison of direct and indirect measures of gene flow in the bat-pollinated tree Hymenaea courbaril in the dry forest life zone of southwestern Puerto Rico. Intl J Plant Sci 165(3):427–436Google Scholar
  37. 37.
    Dutech C, Seiter J, Petronelli P, Joly HI, Jarne PI (2002) Evidence of low gene flow in a neotropical clustered tree species in two rainforest stands of French Guiana. Mol Ecol 11:725–738.PubMedGoogle Scholar
  38. 38.
    Fedorov AA (1966) The structure of the tropical rain forest and speciation in the humid tropics. J Ecol 54(1):1–11Google Scholar
  39. 39.
    Franceschinelli EV, Bawa KS (2000) The effect of ecological factors on the mating system of a South American shrub species (Helicteres brevispira). Heredity 84(1):116–123PubMedGoogle Scholar
  40. 40.
    Frankie GW, Haber WA (1983) Why bees move among mass-flowering neotropical trees. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Rostrand Reinhold, New York, pp 360–372Google Scholar
  41. 41.
    Fuchs EJ, Lobo JA, Quesada M (2003) Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata. Cons Biol 17(1):149–157Google Scholar
  42. 42.
    Gan YY, Robertson FW, Ashton PS, Soepadmo E, Lee DW (1977) Genetic variation in wild populations of rain-forest trees. Nature 269(5626):323–325Google Scholar
  43. 43.
    Gentry AH (1982) Patterns of neotropical plant species diversity. Evol Biol 15:1–84Google Scholar
  44. 44.
    Givnish TJ (1999) On the causes of gradients in tropical tree diversity. J Ecol 87:193–210Google Scholar
  45. 45.
    Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Ann Rev Ecol Evol Syst 36:47–79Google Scholar
  46. 46.
    Gribel R, Lemes MR (1997) Mating system and pollen flow of Ceiba pentandra (Bombacaceae) in Central Amazon Assessment of levels and dynamics of intra-specific genetic diversity of tropical trees. Second Annual Report to the European Commission.Google Scholar
  47. 47.
    Hall P, Orrell L, Bawa KS (1994) Genetic diversity and mating system in a tropical tree, Carapa guianensis (Meliaceae). Am J Bot 81(9):1104–1111Google Scholar
  48. 48.
    Hall P, Walker S, Bawa KS (1996) Effect of forest fragmentation on genetic diversity and mating system in a tropical tree, Pithecellobium elegans. Cons Biol 10(3):757–768Google Scholar
  49. 49.
    Hamilton MB, 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(4):1897–1909PubMedGoogle Scholar
  50. 50.
    Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Man 197(1–3):323–335Google Scholar
  51. 51.
    Hamrick JL, Loveless MD (1989) Genetic structure of tropical tree populations: associations with reproductive biology. In: Bock JH, Linhart YB (eds) Evolutionary ecology of plants. Westview, Boulder, pp 129–146Google Scholar
  52. 52.
    Hamrick JL, Murawski DA (1990) The breeding structure of tropical tree populations. Plant Spec Biol 5:157–165Google Scholar
  53. 53.
    Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Phil Trans Roy Soc Lond Ser B Biol Sci 351(1345):1291–1298Google Scholar
  54. 54.
    Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forests 6:95–124Google Scholar
  55. 55.
    Hardesty BD, Dick CW, Kremer A, Hubbell SP, Bermingham E (2005) Spatial genetic structure of Simarouba amara Aubl. (Simaroubaceae), a dioecious, animal dispersed tree, on Barro Colorado Island, Panama. Heredity 95:290–297PubMedGoogle Scholar
  56. 56.
    Hardesty BD, Hubbell SP, Bermingham E (2006) Genetic evidence of frequent long-distance recruitment in a vertebrate-dispersed tree. Ecol Let 9(5):516–525Google Scholar
  57. 57.
    Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier MH, Doligez A, Dutech C, Kremer A, Latouche-Halle C, Troispoux V, Veron V, Degen B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15(2):559–571PubMedGoogle Scholar
  58. 58.
    Heuertz M, Vekemans X, Hausman JF, Palada M, Hardy OJ (2003) Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash. Mol Ecol 12(9):2483–2495PubMedGoogle Scholar
  59. 59.
    Howe HF (1977) Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58(3):539–550Google Scholar
  60. 60.
    Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228Google Scholar
  61. 61.
    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  62. 62.
    Hubbell SP, Foster RB (1983) Diversity of canopy trees in a neotropical forest and implications for conservation. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forest: ecology and management. Blackwell Scientific, Oxford, pp 25–41Google Scholar
  63. 63.
    Hufford KM, Hamrick JL (2003) Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57(3):518–526PubMedGoogle Scholar
  64. 64.
    Hurtt GC, Pacala SW (1995) The consequences of recruitment limitation - reconciling chance, history and competitive differences between plants. J Theor Biol 176(1):1–12Google Scholar
  65. 65.
    Janzen DH (1967) Synchronization of sexual reproduction of trees within dry season in Central America. Evolution 21(3):620–637Google Scholar
  66. 66.
    Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528Google Scholar
  67. 67.
    Jones FA, Hubbell SP (2006) Demographic spatial genetic structure of the Neotropical tree, Jacaranda copaia. Mol Ecol 15(11):3205–3217PubMedGoogle Scholar
  68. 68.
    Jones FA, Chen J, Weng G-J, Hubbell SP (2005) A genetic evaluation of seed dispersal in the neotropical tree Jacaranda copaia (Bignoniaceae). Am Nat 166(5):543–555PubMedGoogle Scholar
  69. 69.
    Jordano P, Garcia C et al (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci U S A 104(9):3278–3282PubMedGoogle Scholar
  70. 70.
    Kenta T, Isagi Y, Nakagawa M, Yamashita M, Nakashizuka T (2004) Variation in pollen dispersal between years with different pollination conditions in a tropical emergent tree. Mol Ecol 13(11):3575–3584PubMedGoogle Scholar
  71. 71.
    Koeniger N, Koeniger G (1980) Observations and experiments on migration and dance communication of Apis dorsata in Sri Lanka. J Apic Res 19:21–34Google Scholar
  72. 72.
    Konuma A, Tsumura Y, Lee CT, Lee SL, Okuda T (2000) Estimation of gene flow in the tropical-rainforest tree Neobalanocarpus heimii (Dipterocarpaceae), inferred from paternity analysis. Mol Ecol 9(11):1843–1852PubMedGoogle Scholar
  73. 73.
    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(5):1055–1064PubMedGoogle Scholar
  74. 74.
    Lee SL (2000) Mating system parameters of Dryobalanops aromatica Gaertn. f. (Dipterocarpaceae) in three different forest types and a seed orchard. Heredity 85(4):338–345PubMedGoogle Scholar
  75. 75.
    Leigh EG, Davidar P, Dick CW, Puyravaud J-P, Terborgh J, Ter Steege H, Wright SJ (2004) Why do some tropical forests have so many kinds of trees? Biotropica 36(4):447–473Google Scholar
  76. 76.
    Levin DA, Kerster HW (1968) Local gene dispersal in Phlox. Evolution 22:130–139Google Scholar
  77. 77.
    Liengsiri C, Boyle TJB, Yeh FC (1998) Mating system in Pterocarpus macrocarpus Kurz in Thailand. J Hered 89(3):216–221Google Scholar
  78. 78.
    Linskens HF (1996) No airborne pollen within tropical rain forests. Proc Koninklijke Nederlandse Akademie Van Wetenschappen 99(3–4):175–180Google Scholar
  79. 79.
    Lobo JA, Quesada M, Stoner KE, Fuchs EJ, Herrerias-Diego Y, Rojas J, Saborio G (2003) Factors affecting phenological patterns of bombacaceous trees in seasonal forests in Costa Rica and Mexico. Am J Bot 90(7):1054–1063Google Scholar
  80. 80.
    Lobo JA, Quesada M, Stoner KE (2005) Effects of pollination by bats on the mating system of Ceiba pentandra (Bombacaceae) populations in two tropical life zones in Costa Rica. Am J Bot 92(2):370–376Google Scholar
  81. 81.
    Lourmas M, Kjellberg F, Dessard H, Joly HI, Chevallier MH (2007) Reduced density due to logging and its consequences on mating system and pollen flow in the African mahogany Entandrophragma cylindricum. Heredity 99:151–160PubMedGoogle Scholar
  82. 82.
    Loveless MD, Hamrick JL, Foster RB (1998) Population structure and mating system in Tachigali versicolor, a monocarpic neotropical tree. Heredity 81:134–143Google Scholar
  83. 83.
    Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95(4):255–273PubMedGoogle Scholar
  84. 84.
    Matallana G, Wendt T, Araugo DSD, Scarano FR (2005) High abundance of dioecious plants in a tropical coastal vegetation. Am J Bot 92(9):1513–1519Google Scholar
  85. 85.
    Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85(10):1477–1501Google Scholar
  86. 86.
    Muellner AN, Savolainen V, Samuel R, Chase MW (2006) The mahogany family “out-of-Africa”: Divergence time estimation, global biogeographic patterns inferred from plastid rbcL DNA sequences, extant, and fossil distribution of diversity. Mol Phyl Evol 40(1):236–250Google Scholar
  87. 87.
    Murawski DA, Hamrick JL (1991) The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67:167–174Google Scholar
  88. 88.
    Murawski DA, Hamrick JL (1992) The mating system of Cavanillesia platanifolia under extremes of flowering tree density: a test of predictions. Biotropica 24:99–101Google Scholar
  89. 89.
    Murawski DA, Gunatilleke IAUN, Bawa KS (1994) The effects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka. Cons Biol 8(4):997–1002Google Scholar
  90. 90.
    Murray KG (1988) Avian seed dispersal of three neotropical gap-dependent plants. Ecol Mon 58:271–98Google Scholar
  91. 91.
    Nason JD, Hamrick JL (1997) Reproductive and genetic consequences of forest fragmentation: Two case studies of neotropical canopy trees. J Hered 88(4):264–276Google Scholar
  92. 92.
    Nason JD, Herre EA, Hamrick JL (1996) Paternity analysis of the breeding structure of strangler fig populations: Evidence for substantial long-distance wasp dispersal. J Biog 23(4):501–512Google Scholar
  93. 93.
    Nason JD, Herre EA, Hamrick JL (1998) The breeding structure of a tropical keystone plant resource. Nature 391(6668):685–687Google Scholar
  94. 94.
    Nathan R (2006) Long distance dispersal of plants. Science 313:786–788PubMedGoogle Scholar
  95. 95.
    Nettel A, Dodd RS (2007) Drifting propagules and receding swamps: Genetic footprints of mangrove recolonization and dispersal along tropical coasts. Evolution 61(4):958–971PubMedGoogle Scholar
  96. 96.
    Obayashi K, Tsumura Y, Ihara-Ujino T, Niiyama K, Tanouchi H, Suyama Y, Washitani I, Lee CT, Lee SL, Muhammad N (2002) Genetic diversity and outcrossing rate between undisturbed and selectively logged forests of Shorea curtisii (Dipterocarpaceae) using microsatellite DNA analysis. International J Plant Sci 163(1):151–158Google Scholar
  97. 97.
    Pacheco LF, Simonetti JA (2000) Genetic structure of a mimosoid tree deprived of its seed disperser, the spider monkey. Cons Biol 14(6):1766–1775Google Scholar
  98. 98.
    Pennington RT, Dick CW (2004) The role of immigrants in the assembly of the South American rainforest tree flora. Phil Trans Roy Soc Lond Ser B Biol Sci 359:1611–1622Google Scholar
  99. 99.
    Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Ann Rev Ecol Evol Syst 37:187–214Google Scholar
  100. 100.
    Petit RJ, Duminil J, Fineschi S, Hempe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14(3):689–701PubMedGoogle Scholar
  101. 101.
    Quesada M, Stoner KE, Lobo JA, Herrerias-Diego Y, Palacios-Guevara C, Munguia-Rosas MA, Salazar KAO, Rosas-Guerrero V (2004) Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated bombacaceous trees. Biotropica 36(2):131–138Google Scholar
  102. 102.
    Ramirez N (2004) Ecology of pollination in a tropical Venezuelan savanna. Plant Ecol 173(2):171–189Google Scholar
  103. 103.
    Regal P (1977) Ecology and evolution of flowering plant dominance. Science 196:622–629PubMedGoogle Scholar
  104. 104.
    Renner SS (2004) Plant dispersal across the tropical Atlantic by wind and sea currents. Intl J Plant Sci 165(4 Suppl.):S23–S33Google Scholar
  105. 105.
    Renner SS (2005) Relaxed molecular clocks for dating historical plant dispersal events. Tree 10(11):550–556Google Scholar
  106. 106.
    Ricklefs RE (2004) A comprehensive framework for global patterns in biodiversity. Ecol Let 7:1–15Google Scholar
  107. 107.
    Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2006) A new method of estimating the pollen dispersal curve independently of effective density. Genetics 173(2):1033–1045PubMedGoogle Scholar
  108. 108.
    Rocha OJ, Aguilar G (2001) Variation in the breeding behavior of the dry forest tree Enterolobium cyclocarpum (Guanacaste) in Costa Rica. Am J Bot 88(9):1600–1606Google Scholar
  109. 109.
    Roesel CS, Kress WJ, Bowdich BM (1996) Low levels of genetic variation in Phenakospermum guyannense (Strelitziaceae), a widespread, bat-pollinated Amazonian herb. Plant Syst Evol 199:1–15Google Scholar
  110. 110.
    Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T (1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86(10):1414–1436PubMedGoogle Scholar
  111. 111.
    Schemske DW, Lande R (1986) Mode of pollination and selection on mating system—comment. Evolution 40(2):436–436Google Scholar
  112. 112.
    Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 108:15–29Google Scholar
  113. 113.
    Sezen UU, Chazdon RL, Holsinger KE (2005) Genetic consequences of tropical second-growth forest regeneration. Science 307(5711):891–891PubMedGoogle Scholar
  114. 114.
    Shapcott A (1999) Vagility and the monsoon rain forest archipelago of northern Australia: Patterns of genetic diversity in Syzygium nervosum (Myrtaceae). Biotropica 31(4):579–590Google Scholar
  115. 115.
    Simpson GG (1940) Mammals and land bridges. J Wash Acad Sci 30:137–163Google Scholar
  116. 116.
    Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecol Man 197(1–3):21–38Google Scholar
  117. 117.
    Smouse PE, Dyer RJ, Westfall RD, Sork VL (2001) Two-generation analysis of pollen flow across a landscape. I. male gamete heterogeneity among females. Evolution 55(2):260–271PubMedGoogle Scholar
  118. 118.
    Stacy EA, Hamrick JL, Nason JD, Hubbell SP, Foster RB, Condit R (1996) Pollen dispersal in low-density populations of three neotropical tree species. Am Nat 148(2):275–298Google Scholar
  119. 119.
    Stephenson AG (1982) When does outcrossing occur in a mass-flowering plant. Evolution 36(4):762–767Google Scholar
  120. 120.
    Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75(1):2–16Google Scholar
  121. 121.
    Turner IM (2001) The ecology of trees in the tropical rain forest. Cambridge University Press, CambridgeGoogle Scholar
  122. 122.
    Valencia R, Foster RB, Villa G, Condit R, Svenning JC, Hernández C, Romoleroux K, Losos E, Magård E, Balslev H (2004) Tree species distributions and local habitat variation in the Amazon: large forest plot in eastern Ecuador. J Ecol 92:214–229Google Scholar
  123. 123.
    Vamosi JC, Otto SP, Barrett SCH (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. J Evol Biol 16(5):1006–1018PubMedGoogle Scholar
  124. 124.
    Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13(4):921–935PubMedGoogle Scholar
  125. 125.
    Veron V, Caron H, Degen B (2005) Gene flow and mating system of the tropical tree Sextonia rubra. Silv Genet 54(6):275–280Google Scholar
  126. 126.
    Wallace AR (1878) Tropical nature and other essays. Macmillan, New YorkGoogle Scholar
  127. 127.
    Wang BC, Sork VL, Leong MT, Smith TB (2007) Hunting of mammals reduces seed removal and dispersal of the afrotropical tree Antrocaryon klaineanum (Anacardiaceae). Biotropica 39(3):340–347Google Scholar
  128. 128.
    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 95:246–254PubMedGoogle Scholar
  129. 129.
    Webb CJ, Bawa KS (1983) Pollen dispersal by hummingbirds and butterflies: a comparative study of two lowland tropical plants. Evolution 37:1258–1270Google Scholar
  130. 130.
    Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130(1):1–14Google Scholar
  131. 131.
    Zarate S, Perez-Nasser N, Casas A (2005) Genetics of wild and managed populations of Leucaena esculenta subsp esculenta (Fabaceae; Mimosoideae) in La Montana of Guerrero, Mexico. Genet Res Crop Evol 52(7):941–957Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Christopher W. Dick
    • 1
    • 2
  • Olivier J. Hardy
    • 3
  • F. Andrew Jones
    • 2
  • Rémy J. Petit
    • 4
  1. 1.Department of Ecology and Evolutionary Biology and HerbariumUniversity of MichiganAnn ArborUSA
  2. 2.Smithsonian Tropical Research InstituteBalboa AncónRepublic of Panama
  3. 3.Behavioural and Evolutionary Ecology UnitUniversité Libre de BruxellesBrusselsBelgium
  4. 4.Institut National de la Recherche AgronomiqueUMR Biodiversity, Genes and CommunitiesCestasFrance

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