Molecular Systematic Analysis Reveals Cryptic Tertiary Diversification of a Widespread Tropical Rain Forest Tree

American Naturalist

Volumn 162, Issue 6, 2003, Pages 691-703

  Dick, Christopher W ^a   Abdul Salim, Kobinah ^b,c   Bermingham, Eldredge ^a  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b HARVARD UNIVERSITY   (United States)

^c NEW YORK BOTANICAL GARDEN   (United States)

Author keywords

Fossils; Internal transcribed spacer (ITS); Long distance dispersal; Molecular clock; Phylogeography; Tropical trees

Indexed keywords

RIBOSOME DNA;

DISPERSAL; GEOGRAPHICAL DISTRIBUTION; PHYLOGEOGRAPHY; RAINFOREST;

AFRICA; ARTICLE; BAYES THEOREM; BIODIVERSITY; CENTRAL AMERICA; COMPARATIVE STUDY; DNA SEQUENCE; FOSSIL; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GUTTIFERAE; HAPLOTYPE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SOUTH AMERICA; TREE;

AFRICA; BASE SEQUENCE; BAYES THEOREM; BIODIVERSITY; CARIBBEAN REGION; CLUSIACEAE; DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; FOSSILS; GEOGRAPHY; HAPLOTYPES; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA; TREES; VARIATION (GENETICS);

CLUSIACEAE; EMBRYOPHYTA; SYMPHONIA GLOBULIFERA;

EID: 0742270764     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/379795     Document Type: Article

References (70)

1. Abdul-Salim, K. 2002. Systematics and biology of Symphonia L. f. (Clusiaceae). Ph.D. diss. Harvard University, Cambridge, Mass.
2. Aide, T. M., and E. Rivera. 1998. Geographic patterns of genetic diversity in Poulsenia armata (Moraceae): implications for the theory of Pleistocene refugia and the importance of riparian forest. Journal of Biogeography 25:695-705.
3. Aldrich, P. R., and J. L. Hamrick. 1998. Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281:103-105.
4. Baldwin, B. G., and M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences of the USA 95:9402-9406.
5. Baldwin, B. G., M. J. Sanderson, J. M. Porter, M. F. Wojciechowski, C. S. Campbell, and M. J. Donoghue. 1995. The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden 82:247-277.
6. Bermingham, E., and C. Dick. 2001. The Inga: newcomer or museum antiquity. Science 293:2214-2216.
7. Bermingham, E., and A. P. Martin. 1998. Comparative mtDNA phylogeography of Neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Molecular Ecology 7:499-517.
8. Bittrich, V., and M. C. E. Amaral. 1996. Pollination biology of Symphonia globulifera (Clusiaceae). Plant Systematics and Evolution 200:101-110.
9. Cavers, S., C. Navarro, and A. J. Lowe. 2003. Chloroplast DNA phylogeography reveals colonization history of a Neotropical tree, Cedrela odorata L., in Mesoamerica. Molecular Ecology 12:1451-1460.
10. Coates, A. G., and J. A. Obando. 1996. The geologic evolution of the Central American isthmus. Pages 21-56 in J. B. C. Jackson, A. F. Budd, and A. G. Coates, eds. Evolution and environment in tropical America. University of Chicago Press, Chicago.
11. Condit, R., N. C. A. Pitman, E. G. Leigh, J. Chave, J. Terborgh, R. B. Foster, P. Nuñez, et al. 2002. Beta-diversity in tropical forest trees. Science 295:666-669.
12. Cortés-Ortiz, L., E. Bermingham, C. Rico, E. Rodriguez-Luna, I. Sampaio, and M. Ruiz-García. 2003. Molecular systematics and biogeography of the Neotropical monkey genus Alouatta. Molecular Phylogenetics and Evolution 26:64-81.
13. Davis, C. C., C. D. Bell, S. Mathews, and M. Donoghue. 2002. Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proceedings of the National Academy of Sciences of the USA 99:6833-6837.
14. Desjardin, J., J.-L. Guillaumet, and G. Mangenot. 1973. Contribution à la connaissance de l'élément non endémique de la flore malgache (végétaux vasculaires). Candollea 28:325-391.
15. Eberhard, J., and E. Bermingham. In press. Phylogeny and biogeography of the Amazona ochrocephala (Aves: Psittacidae) complex. Auk.
16. Felsenstein, J. 1988. Phylogenies from molecular sequences: inference and reliability. Annual Review of Genetics 22:521-565.
17. Fournier, G. R. 1982. Palynostratigraphic analysis of cores from site 493, Deep Sea Drilling Project leg 66. Initial Reports of the Deep Sea Drilling Project 66:661-670.
18. Gautier-Hion, A., J.-M. Duplantier, R. Quris, F. Feer, C. Sourd, J.-P. Decoux, G. Dubost, et al. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia (Berlin) 65:324-337.
19. Gentry, A. 1982. Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of Andean orogeny? Annals of the Missouri Botanical Garden 69:557-593.
20. Gentry, A. H. 1993. Diversity and floristic composition of lowland tropical forest in Africa and South America. Pages 500-547 in P. Goldblatt, ed. Biological relationships between Africa and South America. Yale University Press, New Haven, Conn.
21. Germeraad, J. H., C. A. Hopping, and J. Muller. 1968. Palynology of Tertiary sediments from tropical areas. Review of Palaeobotany and Palynology 6:189-348.
22. Gill, G. E., R. T. Fowler, and S. A. Mori. 1998. Pollination biology of Symphonia globulifera (Clusiaceae) in central French Guiana. Biotropica 30:139-144.
23. Gillies, A. C. M., C. Navarro, A. J. Lowe, A. C. Newton, M. Hernandez, J. Wilson, and J. P. Cornelius. 1999. Genetic diversity in Mesoamerican populations of mahogany (Swietenia macrophylla), assessed using RAPDs. Heredity 83:722-732.
24. Graham, A. 1976. Studies in Neotropical paleobotany. II. The Miocene communities of Veracruz, Mexico. Annals of the Missouri Botanical Garden 63:787-842.
25. Graham, A., and D. L. Dilcher. 1998. Studies in Neotropical paleobotany. XII. A palynoflora from the Pliocene Rio Banano Formation of Costa Rica and the Neogenevegetation of Mesoamerica. American Journal of Botany 85:1426-1438.
26. Gustafson, K. R., J. W. Blunt, M. H. G. Munro, R. W. Fuller, T. C. McKee, J. H. Cardellina, J. B. McMahon, G. M. Cragg, and M. R. Boyd. 1992. HIV-inhibitory natural products. 8. The guttiferones, HIV-inhibitory benzophenones from Symphonia globulifera, Garcinia livingstonei, Garcinia ovalifolia and Clusia rosea. Tetrahedron 48:10093-10102.
27. Gustafsson, M. H. G., and V. Bittrich. 2003. Evolution of morphological diversity and resin secretion in flowers of Clusia (Clusiaceae): insights from ITS sequence variation. Nordic Journal of Botany 22:183-203.
28. Gustafsson, M. H. G., V. Bittrich, and P. F. Stevens. 2002. Phylogeny of Clusiaceae based on rbcL sequences. International Journal of Plant Science 163:1045-1054.
29. Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22:160-174.
30. Holbrook, K. M., and T. B. Smith. 2000. Seed dispersal and movement patterns in two species of Ceratogymna hornbills in a West African tropical lowland forest. Oecologia (Berlin) 125:249-257.
31. Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, N.J.
32. Huelsenbeck, J. P., and F. Ronquist. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754-755.
33. Iturraldi-Vinent, M. A., and R. D. E. MacPhee. 1999. Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bulletin of the American Museum of Natural History 238:1-95.
34. Jan-du-Chene, R. E., M. S. Onyike, and M. A. Sowunmi. 1978. Some new Eocene pollen of the Ogwashi-Asaba Formation, southeastern Nigeria. Revista Espanola de Micropaleontologia 10:285-322.
35. Janzen, D. H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101:233-249.
36. Jørgensen, P. M., and S. León-Yánez. 1999. Catalogue of the vascular plants of Ecuador. Missouri Botanical Garden, St. Louis.
37. Kimura, M. 1981. Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences of the USA 78: 454-458.
38. Lemes, M., R. Gribel, J. Proctor, and D. Grattapaglia. 2003. Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon: implications for conservation. Molecular Ecology 12:2875-2883.
39. Lundberg, J. G., L. G. Marshall, J. Guerrero, B. Horton, M. C. Malabarba, and F. Wesselingh. 1998. The stage for Neotropical fish diversification: a history of tropical south American rivers. Pages 13-48 in L. R. Malabarba, R. E. Reis, R. P. Vari, S. M. Lucena, and C. A. S. Lucena, eds. Phylogeny and classification of Neotropical fishes. Edipucrs, Porto Alegre.
40. MacArthur, R. H. 1972. Geographical ecology. Harper & Row, New York.
41. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4: analysis of phylogeny and character evolution. Version 4.0. Sinauer, Sunderland, Mass.
42. Maury-Lechon, G., F. Corbineau, and D. Côme. 1980. Données préliminaires sur la germination des graines et la conservation des plantules de Symphonia globulifera L. f. (Guttifère). Revue Bois et Forêts des Tropiques 193: 35-40.
43. Morley, R. J. 2000. Origin and evolution of tropical rain forests. Wiley, Chichester.
44. Novick, R. R., C. Dick, M. R. Lemes, C. Navarro, A. Caccone, and E. Bermingham. 2003. Genetic structure of Mesoamerican populations of big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Molecular Ecology 12:2885-2893.
45. Perdices, A., E. Bermingham, A. Montilla, and I. Doadrio. 2002. Evolutionary history of the genus Rhamdia (Teleostei: Pimelodidae) in Central America. Molecular Phylogenetics and Evolution 25:172-189.
46. Pitman, N. C. A., J. Terborgh, M. R. Silman, and P. Nuñez. 1999. Tree species distributions in an upper Amazonian forest. Ecology 80:2651-2661.
47. Posada, D., and K. A. Krandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
48. Raven, P. H. 1999. Foreword. Pages vi-viii in P. M. Jørgensen and S. León-Yánez, eds. Catalogue of the vascular plants of Ecuador. Missouri Botanical Garden, St. Louis.
49. Raven, P. H., and D. I. Axelrod. 1974. Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden 61:539-673.
50. Renner, S. S., G. Clausing, and K. Meyer. 2001. Historical biogeography of Melastomataceae: the roles of tertiary migration and long-distance dispersal. American Journal of Botany 88:1290-1300.
51. Richardson, J. E., R. T. Pennington, T. D. Pennington, and P. M. Hollingsworth. 2001. Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science 293:2242-2245.
52. Ricklefs, R. E., and D. Schluter. 1993. Species diversity: regional and historical influences. Pages 350-363 in R. E. Ricklefs and D. Schluter, eds. Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago.
53. Sanderson, M. J. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution 14:1218-1231.
54. _. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19:101-109.
55. Sang, T., D. J. Crawford, S. Kim, and T. F. Stuessy. 1994. Radiation of the endemic genus Dendroseris (Asteraceae) on the Juan Fernandez Islands: evidence from sequences of the ITS regions of nuclear ribosomal DNA. American Journal of Botany 81:1494-1501.
56. Savard, L., M. Martin, and J. Bousquet. 1993. Genetic diversity and phylogenetic relationships between birches and alders using ITS, 18S rRNA and rbcL gene sequences. Molecular Phylogenetics and Evolution 2:112-118.
57. Scarano, F. R., K. T. Ribeiro, L. F. D. De Moraes, and H. C. De Lima. 1997. Plant establishment on flooded and unflooded patches of a freshwater swamp forest in southeastern Brazil. Journal of Tropical Ecology 13:793-803.
58. Soltis, D. E., P. S. Soltis, V. Savolainen, P. R. Crane, and T. G. Barraclough. 2002. Rate heterogeneity among lineages of tracheophytes: integration of molecular and fossil data and evidence for molecular living fossils. Proceedings of the National Academy of Sciences of the USA 99:4430-4435.
59. Stevens, P. F. In press. Clusiaceae. In K. Kubitzki, ed. The families and genera of flowering plants. Vol. 4. Flowering plants, dicotyledons, dilleniid families. Springer, Heidelberg.
60. Suh, Y., K. Heo, and C. W. Park. 2000. Phylogenetic relationships of maples (Acer L.; Aceraceae) implied by nuclear ribosomal ITS sequences. Journal of Plant Research 113:193-202.
61. Suh, Y. B., L. B. Thien, H. E. Reeve, and E. A. Zimmer. 1993. Molecular evolution and phylogenetic implications of internal transcribed spacer sequences of ribosomal DNA in Winteraceae. American Journal of Botany 80:1042-1055.
62. Swofford, D. S. 1998. Phylogenetic analysis using parsimony, version 4.04b8. Sinauer, Sunderland, Mass.
63. Tavaré, S. 1986. Some probabilistic and statistical problems on the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17:57-86.
64. Urbatsch, L. E., B. G. Baldwin, and M. J. Donoghue. 2000. Phylogeny of the coneflowers and relatives (Heliantheae: Asteraceae) based in nuclear rDNA internal transcribed spacer (ITS) sequences and chloroplast DNA restriction site data. Systematic Botany 25:539-565.
65. Vargas, P., C. M. Morton, and S. L. Jury. 1999. Biogeographic patterns in Mediterranean and Macaronesian species of Saxifraga (Saxifragaceae) inferred from phylogenetic analyses of ITS sequences. American Journal of Botany 86:724-734.
66. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315-322 in T. White, ed. PCR protocols: a guide to methods and application. Academic Press, San Diego, Calif.
67. Whitmore, F. C., and R. H. Stewart. 1965. Miocene mammals and Central American seaways. Science 148:180-185.
68. Whitmore, T. C., and G. Prance. 1987. Biogeography and quaternary history in tropical America. Oxford Science, Clarendon, Oxford.
69. Wright, S. J. 2002. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia (Berlin) 130:1-14.
70. Zamudio, K. R., and H. W. Greene. 1997. Phylogeography of the bushmaster (Lachesis muta: Viperidae): implications for Neotropical biogeography, systematics, and conservation. Biological Journal of the Linnean Society 62:421-442.