'Out-of-Africa' dispersal of tropical floras during the Miocene climatic optimum: Evidence from Uvaria (Annonaceae)

Journal of Biogeography

Volumn 39, Issue 2, 2012, Pages 322-335

  Zhou, Linlin ^a,b   Su, Yvonne C F ^a   Thomas, Daniel C ^a   Saunders, Richard M K ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Africa Asia disjunction; Ancestral area; Angiosperms; Annonaceae; Historical biogeography; Long distance dispersal; Migration; Tropical forests

Indexed keywords

ANCESTRY; BAYESIAN ANALYSIS; CLIMATE VARIATION; DICOTYLEDON; DISJUNCT DISTRIBUTION; DISPERSAL; FLORISTICS; HYPOTHESIS TESTING; HYPSITHERMAL; INDIAN PLATE; MIOCENE; PALEOBOTANY; PALEOTROPICAL KINGDOM; PHYLOGENETICS; PRIMATE; TROPICAL ENVIRONMENT; TROPICAL FOREST; VICARIANCE;

AFRICA; ASIA; AUSTRALASIA;

ANNONACEAE; MAGNOLIOPHYTA; PRIMATES; UVARIA;

EID: 84855778726     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02598.x     Document Type: Article

References (105)

1. Aitchison, J.C., Ali, J.R. & Davis, A.M. (2007) When and where did India and Asia collide? Journal of Geophysical Research, 112. article no. B05423.
2. Akaike, H. (1981) Likelihood of a model and information criteria. Journal of Econometrics, 16, 3-14.
3. Ali, J.R. & Aitchison, J.C. (2008) Gondwana to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through the latest Eocene (166-35Ma). Earth-Science Reviews, 88, 145-166.
4. Ali, J.R. & Huber, M. (2010) Mammalian biodiversity on Madagascar controlled by ocean currents. Nature, 463, 653-656.
5. Andrews, P. & van Couvering, J.A.H. (1975) Palaeoenvironments in the East African Miocene. Approaches to primate paleobiology (ed. by X. Szalay ), pp. 62-103. Contribution to Primate Biology, Vol. 5, Karger, Basel.
6. Antal, J.S. & Prasad, M. (1999) Morphotaxonomic study of some more fossil leaves from the Lower Siwalik sediments of West Bengal, India. Palaeobotanist, 47, 88-98.
7. Au, Y.Y.A. (2006) Patterns of seed predation in the upland landscape of Hong Kong. Unpublished PhD Thesis, The University of Hong Kong, Hong Kong.
8. Auffenberg, W. (1988) Gray's monitor lizard. University of Florida Press, Gainesville, FL.
9. Baum, D.A., Small, R.L. & Wendel, J.F. (1998) Biogeography and floral evolution of baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets. Systematic Biology, 47, 181-207.
10. Beehler, B. (1983) Frugivory and polygamy in birds of paradise. The Auk, 100, 1-12.
11. Birkinshaw, C. (2001) Fruit characteristics of species dispersed by the black lemur (Eulemur macaco) in the Lokobe Forest, Madagascar. Biotropica, 33, 478-486.
12. Britt, A. & Iambana, B.R. (2003) Can captive-bred Varecia variegata adapt to a natural diet on release to the wild? International Journal of Primatology, 24, 987-1005.
13. Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quade, J., Eisenmann, V. & Ehleringer, J.R. (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature, 389, 153-158.
14. Clayton, J.W., Soltis, P.S. & Soltis, D.E. (2009) Recent long-distance dispersal overshadows ancient biogeographical patterns in a pantropical angiosperm family (Simaroubaceae, Sapindales). Systematic Biology, 58, 395-410.
15. Coetzee, J.A. (1978) Climatic and biological changes in south-western Africa during the late Cainozoic. Palaeoecology of Africa, 10, 13-29.
16. Couvreur, T.L.P., Chatrou, L.W., Sosef, M.S.M. & Richardson, J.E. (2008) Molecular phylogenetics reveal multiple Tertiary vicariance origins of the African rain forest trees. BMC Biology, 6, article no. 54.
17. Couvreur, T.L.P., Pirie, M.D., Chatrou, L.W., Saunders, R.M.K., Su, Y.C.F., Richardson, J.E. & Erkens, R.H.J. (2011) Early evolutionary history of the flowering plant family Annonaceae: steady diversification and boreotropical geodispersal. Journal of Biogeography, 38, 664-680.
18. Davis, C.C., Bell, C.D., Fritsch, P.W. & Mathews, S. (2002) Phylogeny of Acridocarpus-Brachylophon (Malpighiaceae): implications for Tertiary tropical floras and Afroasian biogeography. Evolution, 56, 2395-2405.
19. Dayanandan, S., Ashton, P.S., Williams, S.M. & Primack, R.B. (1999) Phylogeny of the tropical tree family Dipterocarpaceae based on nucleotide sequences of the chloroplast rbcL gene. American Journal of Botany, 86, 1182-1190.
20. Dilcher, D.L. & Crane, P.R. (1984) Archaeanthus: an early angiosperm from the Cenomanian of the Western Interior of North America. Annals of the Missouri Botanical Garden, 71, 351-361.
21. Doyle, J.A. & Endress, P.K. (2010) Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. Journal of Systematics and Evolution, 48, 1-35.
22. Doyle, J.A. & Le Thomas, A. (1996) Phylogenetic analysis and character evolution in Annonaceae. Bulletin du Muséum d'Histoire Naturelle, Section B, Adansonia, 18, 85-94.
23. Doyle, J.A. & Le Thomas, A. (1997) Phylogeny and geographic history of Annonaceae. Géographie Physique et Quaternaire, 51, 353-361.
24. Doyle, J.A., Sauquet, H., Scharaschkin, T. & Le Thomas, A. (2004) Phylogeny, molecular and fossil dating, and biogeographic history of Annonaceae and Myristicaceae (Magnoliales). International Journal of Plant Sciences, 165(S4), S55-S67.
25. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, article no. 214.
26. Drummond, A.J. & Rambaut, A. (2008) BEAST version 1.4.8. Available at:
27. Drummond, A.J., Ho, S., Phillips, M. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699-710.
28. Dubost, G. (1984) Comparison of the diets of frugivorous forest ruminants of Gabon. Journal of Mammalogy, 65, 298-316.
29. Dunbar, R.I.M. (1974) Observations on the ecology and social organization of the green monkey, Cercopithecus sabaeus, in Senegal. Primates, 15, 341-350.
30. Dutton, J.F. & Barron, E.J. (1997) Miocene to present vegetation changes: a possible piece of the Cenozoic cooling puzzle. Geology, 25, 39-41.
31. Erkens, R.H.J., Maas, J.W. & Couvreur, T.L.P. (2009) From Africa to South America: migrational route of a species-rich genus of Neotropical lowland rain forest trees (Guatteria, Annonaceae). Journal of Biogeography, 36, 2338-2352.
32. Fleagle, J.G. & Gilbert, C.C. (2006) The biogeography of primate evolution: the role of plate tectonics, climate and chance. Primate biogeography: progress and prospects (ed. by S.M. Lehman and J.G. Fleagle ), pp. 374-417. Springer, New York.
33. Frith, C.B. & Beehler, B.M. (1998) The birds of paradise: Paradisaeidae. Oxford University Press, Oxford.
34. Gautier-Hion, A., Emmons, L.H. & Dubost, G. (1980) A comparison of the diets of three major groups of primary consumers of Gabon (primates, squirrels and ruminants). Oecologia, 45, 182-189.
35. Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., Moungazi, A., Roussilhon, C. & Thiollay, J.-M. (1985) Fruit characters as a basis for fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65, 324-337.
36. Gregor, H.-J. (1977) Subtropische Elemente im europäischen Tertiär II (Fruktifikationen). Paläontologische Zeitschrift, 51, 199-226.
37. Hall, R. (2001) Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. Faunal and floral migrations and evolution in SE Asia-Australasia (ed. by I. Metcalfe, J.M.B. Smith, M. Morwood and I.D. Davidson ), pp. 35-56. Swets & Zeitlionger, Lisse.
38. Hall, R. (2009) Southeast Asia's changing palaeogeography. Blumea, 54, 148-161.
39. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
40. Harcourt, C.S. & Nash, L.T. (1986) Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates, 27, 41-52.
41. Ho, S.Y.W. & Phillips, M.J. (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Systematic Biology, 58, 367-380.
42. Ho, W.P. (2009) The role of masked palm civet (Paguma larvata) and small Indian civet (Viverricula indica) in seed dispersal in Hong Kong, China. Unpublished PhD Thesis, The University of Hong Kong, Hong Kong.
43. Jacobs, B.F. (2004) Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 1573-1583.
44. Jacobs, L.L. (1981) Miocene lorisid primates from the Pakistan Siwaliks. Nature, 289, 585-587.
45. Karanth, K.P. (2003) Evolution of disjunct distributions among wet-zone species of the Indian subcontinent: testing various hypotheses using a phylogenetic approach. Current Science, 85, 1276-1283.
46. Kemp, A. (1995) The hornbills: Bucerotiformes. Oxford University Press, Oxford.
47. Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Maruhashi, T. & Noma, N. (2002) Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia, 133, 559-572.
48. Kitamura, S., Yumoto, T., Noma, N., Chuailua, P., Maruhashi, T., Wohandee, P. & Poonswad, P. (2008) Aggregated seed dispersal by wreathed hornbills at a roost site in a moist evergreen forest of Thailand. Ecological Research, 23, 943-952.
49. Kulju, K.K.M., Sierra, S.E.C., Draisma, S.G.A., Samuel, R. & van Welzen, P.C. (2007) Molecular phylogeny of Macaranga, Mallotus, and related genera (Euphorbiaceae s.s.): insights from plastid and nuclear DNA sequence data. American Journal of Botany, 94, 1726-1743.
50. Kunz, B.K. & Linsenmair, K.E. (2008) Seed size selection by olive baboons. Primates, 49, 239-245.
51. Leighton, M. & Leighton, D.R. (1983) Vertebrate responses to fruiting seasonality within a Bornean rain forest. Tropical rain forest: ecology and management (ed. by S.L. Sutton, T.C. Whitmore and A.C. Chadwick ), pp. 181-196. Blackwell, Oxford.
52. Li, Y., Dressler, S., Zhang, D. & Renner, S.S. (2009) More Miocene dispersal between Africa and Asia - the case of Bridelia (Phyllanthaceae). Systematic Botany, 34, 521-529.
53. Lieberman, D., Hall, J.B., Swaine, M.D. & Lieberman, M. (1979) Seed dispersal by baboons in the Shai Hills, Ghana. Ecology, 60, 65-75.
54. Lieberman, M. & Lieberman, D. (1986) An experimental study of seed ingestion and germination in a plant-animal assemblage in Ghana. Journal of Tropical Ecology, 2, 113-126.
55. MacPhee, R.D.E. & Jacobs, L.L. (1986) Nycticeboides simpsoni and the morphology, adaptations, and relationship of Miocene Siwalik Lorisidae. Contributions to Geology, University of Wyoming, Special Paper, 3, 131-161.
56. Maddison, W.P. & Maddison, D.R. (2010) Mesquite: a molecular system for evolutionary analysis, version 2.7.4. Available at:
57. Mai, D.H. (1970) Subtropische Elemente im europäischen Tertiare. Paläontologische Abhandlungen. Abteilung B, Paläobotanik, 3, 441-503.
58. Malcomber, S.T. (2002) Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus. Evolution, 56, 42-57.
59. Mohr, B.A.R. & Bernardes-de-Oliveira, M.E.C. (2004) Endressinia brasiliana, a magnolialean angiosperm from the Lower Cretaceous Crato Formation (Brazil). International Journal of Plant Sciences, 165, 1121-1133.
60. Morley, R.J. (2000) Origin and evolution of tropical rain forests. John Wiley, New York.
61. Morley, R.J. (2007) Cretaceous and Tertiary climate change and the past distribution of megathermal rainforests. Tropical rainforest responses to climate changes (ed. by M.B. Bush and J. Flenley ), pp. 1-31. Praxis, Chichester, UK.
62. Moscovice, L.R., Issa, M.H., Petrzelkova, K.J., Keuler, N.S., Snowdon, C.T. & Huffman, M.A. (2007) Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania. American Journal of Primatology, 69, 487-502.
63. Muellner, A.N., Savolainen, V., Samuel, R. & Chase, M.W. (2006) The mahogany family "out-of-Africa": divergence time estimation, global biogeographic patterns inferred from plastid rbcL DNA sequences, extant, and fossil distributions of diversity. Molecular Phylogenetics and Evolution, 40, 236-250.
64. Muellner, A.N., Pannell, C.M., Coleman, A. & Chase, M.W. (2008) The origin and evolution of Indomalesian, Australasian and Pacific Island biotas: insights from Aglaieae (Meliaceae, Sapindales). Journal of Biogeography, 35, 1769-1789.
65. Nishida, T. (1972) A note on the ecology of the red-colobus monkeys (Colobus badius tephrosceles) living in the Mahali Mountains. Primates, 13, 57-64.
66. Nishida, T. & Uehara, S. (1983) Natural diet of chimpanzees (Pan troglodytes schweinfurthii): long-term record from the Mahale Mountains, Tanzania. African Study Monographs, 3, 109-130.
67. Nylander, J.A.A. (2004) MrModeltest, version 2. Evolutionary Biology Centre, Uppsala University, Uppsala. Available at:
68. Nylander, J.A.A., Olsson, U., Alstrom, P. & Sanmartín, I. (2008) Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Systematic Biology, 57, 257-268.
69. Peignot, P., Charpentier, M.J.E., Bout, N., Bourry, O., Massima, U., Dosimont, O., Terramorsi, R. & Wickings, E.J. (2008) Learning from the first release project of captive-bred mandrills Mandrillus sphinx in Gabon. Oryx, 42, 122-131.
70. Pirie, M.D., Chatrou, L.W., Mols, J.B., Erkens, R.H.J. & Oosterhof, J. (2006) 'Andean-centred' genera in the short-branch clade of Annonaceae: testing biogeographical hypotheses using phylogeny reconstruction and molecular dating. Journal of Biogeography, 33, 31-46.
71. Prasad, M. (1994) Siwalik (Middle Miocene) leaf impressions from the foot-hills of Himalayas, India. Tertiary Research, 15, 53-90.
72. Rabinowitz, P.D., Coffin, M.F. & Falvey, D. (1983) The separation of Madagascar and Africa. Science, 220, 67-69.
73. Rambaut, A. (1996) Se-Al: Sequence Alignment Editor, version 2.0. Available at:
74. Rambaut, A. (2009) FigTree version 1.3.0. Available at:
75. Rambaut, A. & Drummond, A.J. (2007) Tracer, version 1.4. Available at:
76. Renner, S.S. (2004) Multiple Miocene Melastomataceae dispersal between Madagascar, Africa, and India. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 1485-1494.
77. Renner, S.S. & Meyer, K. (2001) Melastomataceae come full circle: biogeographic reconstruction and molecular clock dating. Evolution, 55, 1315-1324.
78. Richardson, J.E., Chatrou, L.W., Mols, J.B., Erkens, R.H.J. & Pirie, M.D. (2004) Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philosophical Transactions of the Royal Society of London, B, 359, 1495-1508.
79. Rogers, M.E., Maisels, F., Williamson, E.A., Fernandez, M. & Tutin, C.E.G. (1990) Gorilla diet in the Lopé Reserve, Gabon. Oecologia, 84, 326-339.
80. Rögl, F. (1998) Palaeogeographic considerations for Mediterranean and Paratethys seaways (Oligocene to Miocene). Annalen des Naturhistorischen Museums in Wien, 99, 279-310.
81. Rögl, F. (1999) Circum-Mediterranean Miocene paleogeography. The Miocene land mammals of Europe (ed. by G. Rössner and K. Heissig ), pp. 39-48. Dr. Fritz Pfeil Verlag, Munich.
82. Ronquist, F. (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195-203.
83. Scharaschkin, T. & Doyle, J.A. (2005) Phylogeny and historical biogeography of Anaxagorea (Annonaceae) using morphology and non-coding chloroplast sequence data. Systematic Botany, 30, 712-735.
84. Schettino, A. & Scotese, C.R. (2001) New internet software aids paleomagnetic analysis and plate tectonic reconstructions. EoS Transactions, American Geophysical Union, 82, 530-536.
85. Schott, F.A., Xie, S.-P. & McCreary, J.P., Jr (2009) Indian Ocean circulation and climate variability. Reviews of Geophysics, 47, RG1002.
86. Shepherd, V.E. & Chapman, C.A. (1998) Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal of Tropical Ecology, 14, 199-215.
87. Sourd, C. & Gautier-Hion, A. (1986) Fruit selection by a forest guenon. Journal of Animal Ecology, 55, 235-244.
88. Su, S. & Sale, J. (2007) Niche differentiation between Common Palm Civet Paradoxurus hermaphroditus and Small Indian Civet Viverricula indica in regenerating degraded forest, Myanmar. Small Carnivore Conservation, 36, 30-34.
89. Su, Y.C.F. & Saunders, R.M.K. (2009) Evolutionary divergence times in the Annonaceae: evidence of a Late Miocene origin of Pseuduvaria in Sundaland with subsequent diversification in New Guinea. BMC Evolutionary Biology, 9, article no. 153.
90. Surveswaran, S., Wang, R.J., Su, Y.C.F. & Saunders, R.M.K. (2010) Generic delimitation and historical biogeography in the early-divergent 'ambavioid' lineage of Annonaceae: Cananga, Cyathocalyx and Drepananthus. Taxon, 59, 1721-1734.
91. Suzuki, A. (1969) An ecological study of chimpanzees in a savanna woodland. Primates, 10, 103-148.
92. Takahashi, M., Friis, E.M., Uesugi, K., Suzuki, Y. & Crane, P.R. (2008) Floral evidence of Annonaceae from the Late Cretaceous of Japan. International Journal of Plant Sciences, 169, 908-917.
93. Tao, J.R. (2000) The evolution of the Late Cretaceous-Cenozoic floras in China. Science Press, Beijing.
94. Tao, J.R. & Chen, M.H. (1983) Neogene flora of south part of the watershed of Salween-Mekong-Yangtze Rivers (the Lin-cang region), Yunnan. Comprehensive scientific expedition to the Qinghai-Xizang Plateau. Studies in Qinghai-Xiazang plateau-special issue of Hengduan mountain scientific expedition (ed. by Chinese Academy of Science), pp. 74-89. Yunnan People's Press, Kunming.
95. Tutin, C.E.G., Williamson, E.A., Rogers, M.E. & Fernandez, M. (1991) A case study of a plant-animal relationship: Cola lizae and lowland gorillas in the Lopé Reserve, Gabon. Journal of Tropical Ecology, 7, 181-199.
96. Warren, B.H., Strasberg, D., Bruggemann, J.H., Prys-Jones, R.P. & Thébaud, C. (2010) Why does the biota of the Madagascar region have such a strong Asiatic flavour? Cladistics, 26, 526-538.
97. Weeks, A., Daly, D.C. & Simpson, B.B. (2005) The phylogenetic history and biogeography of the frankincense and myrrh family (Burseraceae) based on nuclear and chloroplast sequence data. Molecular Phylogenetics and Evolution, 35, 85-101.
98. Whybrow, P.J. & Andrews, P. (2000) Response of Old World terrestrial vertebrate biotas to Neogene climate change. Biotic response to global change: the last 145 million years (ed. by S.J. Culver and P.F. Rawson ), pp. 350-366. Cambridge University Press, New York.
99. Wolfe, J.A. (1975) Some aspects of plant geography of the Northern Hemisphere during the Late Cretaceous and Tertiary. Annals of the Missouri Botanical Garden, 62, 264-279.
100. Yu, Y., Harris, A.J. & He, X. (2010a) S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56, 848-850.
101. Yu, Y., Harris, A.J. & He, X. (2010b) S-DIVA (Statistical Dispersal-Vicariance Analysis), version 1.9 beta. Available at:
102. Yuan, Y.M., Wohlhauser, S., Möller, M., Klackenberg, J., Callmander, M.W. & Küpfer, P. (2005) Phylogeny and biogeography of Exacum (Gentianaceae): a disjunctive distribution in the Indian Ocean basin resulted from long distance dispersal and extensive radiation. Systematic Biology, 54, 21-34.
103. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. (2001) Trends, rhythms, and aberration in global climate 65Ma to present. Science, 292, 686-693.
104. Zhou, L.L., Su, Y.C.F. & Saunders, R.M.K. (2009) Molecular phylogenetic support for a broader delimitation of Uvaria (Annonaceae), inclusive of Anomianthus, Cyathostemma, Ellipeia, Ellipeiopsis and Rauwenhoffia. Systematics and Biodiversity, 7, 249-258.
105. Zhou, L.L., Su, Y.C.F., Chalermglin, P. & Saunders, R.M.K. (2010) Molecular phylogenetics of Uvaria (Annonaceae): relationships with Balonga, Dasoclema and Australian species of Melodorum. Botanical Journal of the Linnean Society, 163, 33-43.