Neoendemism in Madagascan scaly tree ferns results from recent, coincident diversification bursts

Evolution

Volumn 62, Issue 8, 2008, Pages 1876-1889

  Janssen, Thomas ^a,b,e   Bystriakova, Nadia ^c   Rakotondrainibe, France ^b   Coomes, David ^c   Labat, Jean Noël ^b   Schneider, Harald ^a,d  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^e SENCKENBERG RESEARCH INSTITUTE   (Germany)

Author keywords

Alsophila; Climatic trigger; Cyathea; Cyatheaceae; Pliocene; Rapid radiation; Western Indian Ocean

Indexed keywords

DNA;

ADAPTIVE RADIATION; ANCESTRY; ANGIOSPERM; ANIMAL; BIOCLIMATOLOGY; CLADISTICS; CLIMATE EFFECT; COLONIZATION; DIVERGENCE; ENDEMIC SPECIES; ENDEMISM; EVERGREEN FOREST; FERN; GONDWANA; MIOCENE; PLIOCENE; RAINFOREST; SPECIES RICHNESS;

ARTICLE; BIOLOGICAL MODEL; CLIMATE; ECOLOGY; EVOLUTION; FERN; FOSSIL; GENETICS; GEOGRAPHY; MADAGASCAR; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; STATISTICAL MODEL; THEORETICAL MODEL; TIME;

CLIMATE; DNA; ECOLOGY; EVOLUTION; FERNS; FOSSILS; GEOGRAPHY; LIKELIHOOD FUNCTIONS; MADAGASCAR; MODELS, GENETIC; MODELS, THEORETICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; TIME FACTORS;

INDIAN OCEAN; INDIAN OCEAN ISLANDS; MADAGASCAR;

ALSOPHILA (FERN); ANIMALIA; CYATHEA; CYATHEACEAE; FILICOPHYTA; MAGNOLIOPHYTA;

EID: 47749146540     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00408.x     Document Type: Article

References (92)

1. Aldasoro, J. J., F. Cabezas, and C. Aedo. 2004. Diversity and distribution of ferns in sub-Saharan Africa, Madagascar and some islands of the South Atlantic. J. Biogeogr. 31 : 1579 1604.
2. Austin, J. J., E. N. Arnold, and C. G. Jones. 2004. Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene Islands. Mol. Phylogenet. Evol. 31 : 109 122.
3. Baldwin, B. G., and M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA 95 : 9402 9406.
4. Biju, S. D., and F. Bossuyt. 2003. New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature 425 : 711 714.
5. Bonfield, J. K., K. F. Smith, and R. Staden. 1995. A new DNA sequence assembly program. Nucleic Acids Res. 24 : 4992 4999.
6. Bramley, G., R. T. Pennington, R. Zakaria, S. S. Tjitrosoedirdjo, and Q. C. B. Cronk. 2004. Assembly of tropical plant diversity on a local scale: Cyrtandra (Gesneriaceae) on Mount Kerinci, Sumatra. Biol. J. Linn. Soc. 81 : 49 62.
7. Collinson, M. E. 1996. What use are fossil ferns? - 20 years on: with a review of the fossil history of extant pteridophyte families and genera. Pp. 349 394 in J. M. Camus, M. Gibby, and R. J. Johns, eds. Pteridology in perspective. Royal Botanical Gardens, Kew.
8. Conant, D. S. 1983. A revision of the genus Alsophila (Cyatheaceae) in the Americas. J. Arnold Arbor 64 : 333 382.
9. Coomes, D. A., R. B. Allen, W. A. Bentley, L. E. Burrows, C. D. Canham, L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, W. A. Ruscoe, et al. 2005. The hare, the tortoise and the crocodile: the ecology of angiosperm dominance, conifer persistence and fern filtering. J. Ecol. 93 : 918 935.
10. Davis, C. C., C. D. Bell, P. W. Fritsch, and S. Mathews. 2002. Phylogeny of Acridocarpus-Brachylophon (Malpighiaceae): implications for tertiary tropical floras and AfroAsian biogeography. Evolution 56 : 2395 2405.
11. Doledec, S., D. Chessel, and C. Gimaret-Carpentier. 2000. Niche separation in community analysis: a new method. Ecology 81 : 2914 2927.
12. DuPuy, D. J., and J. Moat. 1999. Vegetation mapping and biodiversity conservation in Madagascar using geographical information systems. Pp. 245 251 in J. Timberlake, and S. Kativu, eds. African plants: biodiversity, taxonomy and uses. Royal Botanic Gardens, Kew.
13. Ebihara, A., K. Iwatsuki, T. A. Ohsawa, and M. Ito. 2003. Hymenophyllum paniense (Hymenophyllaceae), a new species of filmy fern from New Caledonia. Syst. Bot. 28 : 228 235.
14. Fjeldså, J., and J. C. Lovett. 1997. Geographical patterns of old and young species in African forest biota: the significance of specific montane areas as evolutionary centres. Biodivers. Conserv. 6 : 325 346.
15. Gasse, F., and E. van Campo. 2001. Late Quaternary environmental changes from a pollen and diatom record in the southern tropics (Lake Tritrivakely, Madagascar). Palaeogeogr. Palaeoclimatol. Palaeoecol. 167 : 287 308.
16. Gaston, K. J., and T. M. Blackburn. 1996. The tropics as a museum of biological diversity: an analysis of the New World avifauna. Proc. R. Soc. Lond. B 263 : 63 68.
17. Grubb, P. J. 2003. Interpreting some outstanding features of the flora and vegetation of Madgascar. Perspect. Plant Ecol. 6 : 125 146.
18. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Syst. Biol. 52 : 696 704.
19. Haq, B. U., J. Hardenbol, and P. R. Vail. 1987. Chronology of fluctuating sea levels since the Triassic. Science 235 : 1156 1167.
20. Hewitt, G. 2000. The genetic legacy of the Quaternary ice ages. Nature 405 : 907 913.
21. Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25 : 1965 1978.
22. Holmgren, P. K., N. H. Holmgren, and L. C. Barnett, eds. 1990. Index Herbariorum, Edition 8: Part I. The Herbaria of the World. New York Botanical Garden Press, New York.
23. Holttum, R. E. 1981. The tree ferns of Africa. Kew Bull. 36 : 463 482.
24. Hughes, C. E., and R. J. Eastwood. 2006. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc. Natl. Acad. Sci. USA 103 : 10334 10339.
25. Janssen, T. 2006. A moulding method to preserve tree fern trunk surfaces including remarks on the composition of tree fern herbarium specimens. Fern. Gaz. 17 : 283 295.
26. Janssen, T., and F. Rakotondrainibe. 2006. A revision of the fern family Cyatheaceae in the Mascarene Islands. Adansonia 28 : 213 241.
27. Janssen, T., and F. Rakotondrainibe. 2007. An update of the revision of Cyathea subgen. Alsophila sect. Gymnosphaera (Cyatheaceae) in Madagascar and the Comoros including a discussion of putative hybridization events. Adansonia 29 : 195 213.
28. Janssen, T., and F. Rakotondrainibe. in press. A revision of the indusiate scaly tree ferns (Cyatheaceae: Cyathea subgen. Alsophila sect. Alsophila) in Madagascar, the Comoros and the Seychelles. Adansonia.
29. Jones, M. M., P. Olivas Rojas, H. Tuomisto, and D. B. Clark. 2007. Environmental and neighbourhood effects on tree fern distributions in a Neotropical lowland rain forest. J. Veg. Sci. 18 : 13 24.
30. Klak, C., G. Reeves, and T. Hedderson. 2004. Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427 : 63 65.
31. Kocher, T. D. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5 : 288 298.
32. Korall, P., K. M. Pryer, J. Metzgar, H. Schneider, and D. S. Conant. 2006. Tree ferns: monophyletic groups and their relationships as revealed by four protein-coding plastid loci. Mol. Phylogenet. Evol. 39 : 830 845.
33. Korall, P., D. S. Conant, J. S. Metzgar, H. Schneider, and K. M. Pryer. 2007. A molecular phylogeny of scaly tree ferns (Cyatheaceae). Am. J. Bot. 94 : 873 886.
34. Kurmann, M. H., and T. N. Taylor. 1987. Sporoderm ultrastructure of Lophosoria and Cyatheacidites (Filicopsida): systematic and evolutionary implications. Plant Syst. Evol. 157 : 85 94.
35. Langley, C. H., and W. M. Fitch. 1974. Examination of constancy of rate of molecular evolution. J. Mol. Evol. 3 : 161 177.
36. Lantz, T. C., G. W. Rothwell, and R. A. Stockey. 1999. Conantiopteris schuchmanii, gen. et sp. nov., and the role of fossils in resolving the phylogeny of Cyatheaceae s.l. J. Plant Res. 112 : 361 381.
37. Linder, H. P., C. R. Hardy, and F. Rutschmann. 2005. Taxon sampling effects in molecular clock dating: an example from the African Restionaceae. Mol. Phylogenet. Evol. 35 : 569 582.
38. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4.05: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA.
39. Maddison, W. P., and D. R. Maddison. 2006a. Mesquite: a modular system for evolutionary analysis2. Version 1.1. http://mesquiteproject.org.
40. Maddison, W. P., and D. R. Maddison. 2006b. StockChar: a package of Mesquite modules for stochastic models of character evolution. Version 1.1. http://mesquiteproject.org.
41. Magallón, S., and M. J. Sanderson. 2001. Absolute diversification rates in angiosperm clades. Evolution 55 : 1762 1780.
42. 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.
43. Mittelbach, G. G., D. W. Schemske, H. V. Cornell, A. P. Allen, J. M. Brown, M. B. Bush, S. B. Harrison, A. H. Hurlbert, N. Knowlton, H. A. Lessios, et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10 : 315 331.
44. Mohr, B. A. R., and B. B. Lazarus. 1994. Paleobiogeographic distribution of Kuylisporites and its possible relationship to the extant fern genus Cnemidaria (Cyatheaceae). Ann. Missouri Bot. Gard. 81 : 759 767.
45. Moritz, C., J. L. Patton, C. J. Schneider, and T. B. Smith. 2000. Diversification of rainforest faunas: an integrated molecular approach. Annu. Rev. Ecol. Syst. 31 : 533 563.
46. Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da Fonseca, and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403 : 853 858.
47. Nylander, J. A. A. 2004. MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala Univ.
48. Pennington, R. T., M. Lavin, D. E. Prado, C. A. Pendry, S. K. Pell, and C. A. Butterworth. 2004. Historical climate change and speciation: Neotropical seasonality dry forest plants show patterns of both Tertiary and Quaternary diversification. Philos. Trans. Ser. B 359 : 515 537.
49. Plana, V., A. Gascoigne, L. L. Forrest, D. Harris, and R. T. Pennington. 2004. Pleistocene and pre-pleistocene Begonia speciation in Africa. Mol. Phylogenet. Evol. 31 : 449 461.
50. Poux, C., O. Madsen, E. Marquard, D. R. Vieites, W. W. de Jong, and M. Vences. 2005. Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst. Biol. 54 : 719 730.
51. Pryer, K. M., E. Schuettpelz, P. G. Wolf, H. Schneider, A. R. Smith, and R. B. Cranfill. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am. J. Bot. 91 : 1582 1598.
52. Rakotondrainibe, F. 2003a. Checklist of the pteridophytes of Madagascar. Pp. 295 313 in S. M. Goodman, and J. P. Benstead, eds. Natural history of Madagascar. The Univ. of Chicago Press, Chicago.
53. Rakotondrainibe, F. 2003b. Diversity, ecology, and distribution of the pteridophyte flora. Pp. 282 295 in S. M. Goodman, and J. P. Benstead, eds. Natural history of Madagascar. The Univ. of Chicago Press, Chicago.
54. Rakotondrainibe, F., and D. Lobreau-Callen. 1999. Révision du genre Cyathea sect. Gymnosphaera (Cyatheaceae) à Madagascar et aux Comores. Adansonia 21 : 137 152.
55. Rambaut, A., and A. Drummond. 2005. Tracer v1.3, Univ. of Oxford, program distributed by the author.
56. Ratcliff, R. 1993. Methods for dealing with reaction time outliers. Psychol. Bull. 114 : 510 532.
57. Raxworthy, C. J., M. R. J. Forstner, and R. A. Nussbaum. 2002. Chameleon radiation by oceanic dispersal. Nature 415 : 784 787.
58. Renner, S. S. 2004. Multiple Miocene Melastomataceae dispersal between Madagascar, Africa and India. Philos. Trans. Ser. B 359 : 1485 1494.
59. 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.
60. Rocha, S., M. A. Carretero, M. Vences, F. Glaw, and D. J. Harris. 2006. Deciphering patterns of transoceanic dispersal: the evolutionary origin and biogeography of coastal lizards (Cryptoblepharus) in the Western Indian Ocean region. J. Biogeogr. 33 : 13 22.
61. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 : 1572 1574.
62. Sanderson, M. J. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14 : 1218 1231.
63. Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19 : 101 109.
64. Sanderson, M. J. 2003. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19 : 301 302.
65. Schneider, H., T. A. Ranker, S. J. Russell, R. B. Cranfill, J. M. O. Geiger, R. Aguraiuja, K. R. Wood, M. Grundmann, K. Kloberdanz, and J. C. Vogel. 2005. Origin of the endemic fern genus Diellia coincides with the renewal of Hawaiian terrestrial life in the Miocene. Proc. R. Soc. Lond. B 272 : 455 460.
66. Schneider, H., E. Schuettpelz, K. M. Pryer, R. B. Cranfill, S. Magallón, and R. Lupia. 2004. Ferns diversified in the shadow of angiosperms. Nature 428 : 553 557.
67. Silvertown, J. 2004. The ghost of competition past in the phylogeny of island endemic plants. J. Ecol. 92 : 168 173.
68. Silvertown, J., J. Francisco-Ortega, and M. Carine. 2005. The monophyly of island radiations: an evaluation of niche pre-emption and some alternative explanations. J. Ecol. 93 : 653 657.
69. Smith, T. B., R. K. Wayne, D. J. Girman, and M. W. Bruford. 1997. A role for ecotones in generating rainforest biodiversity. Science 276 : 1855 1857.
70. Smith, S. Y., G. W. Rothwell, and R. A. Stockey. 2003. Cyathea cranhamii sp. nov. (Cyatheaceae), anatomically preserved tree fern sori from the lower Cretaceous of Vancouver Island, British Columbia. Am. J. Bot. 90 : 755 760.
71. Sparks, J. S., and W. L. Smith. 2004. Phylogeny and biogeography of the Malagasy and Australasian rainbowfishes (Teleostei: Melanotaenioidei): Gondwanan vicariance and evolution in freshwater. Mol. Phylogenet. Evol. 33 : 719 734.
72. Stebbins, G. L. 1974. Flowering plants. Harvard Univ. Press, Cambridge.
73. Swofford, D. L. 2000. PAUP*: phylogenetic analyses using parsimony (* and other methods), version 4b10. Sinauer Associates, Sunderland, MA.
74. Taberlet, P., L. Gielly, G. Pantou, and J. Bouvet. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17 : 1105 1109.
75. Takhtajan, A. 1986. Floristic regions of the world. Univ. of California Press, Berkeley, CA.
76. Thorne, J. L., H. Kishino, and I. S. Painter. 1998. Estimating the rate of evolution of the rate of molecular evolution. Mol. Biol. Evol. 15 : 1647 1657.
77. Thuiller, W., S. Lavorel, G. F. Midgley, S. Lavergne, and A. Rebelo. 2004. Relating plant traits and species distributions along bioclimatic gradients for 88 Leucadendron taxa. Ecology 85 : 1688 1699.
78. Vences, M., J. Freyhof, R. Sonnenberg, J. Kosuch, and M. Veith. 2001. Reconciling fossils and molecules: Cenozoic divergence of chichlid fishes and the biogeography of Madagascar. J. Biogeogr. 28 : 1091 1099.
79. Vences, M., D. R. Vieites, F. Glaw, H. Brinkmann, J. Kosuch, M. Veith, and A. Meyer. 2003. Multiple overseas dispersal in amphibians. Proc. R. Soc. Lond. B. 270 : 2435 2442.
80. Vences, M., S. Wanke, D. R. Vieites, W. R. Branch, F. Glaw, and A. Meyer. 2004. Natural colonization or introduction? Phylogeographical relationships and morphological differentiation of house geckos (Hemidactylus) from Madagascar. Biol. J. Linn. Soc. 83 : 115 130.
81. Warren, B. H., E. Bermingham, R. P. Prys-Jones, and C. Thébaud. 2006. Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands. Mol. Ecol. 15 : 3769 3786.
82. Wells, N. A. 2003. Some hypotheses on the Mesozoic and Cenozoic palaeoenvironmental history of Madagascar. Pp. 16 34 in S. M. Goodman, and J. P. Benstead, eds. Natural history of Madagascar. The Univ. of Chicago Press, Chicago.
83. Whittaker, R. J., and J. M. Fernández-Palacios. 2007. Island Biogeography. 2nd ed. Oxford Univ. Press, Oxford.
84. Wiens, J. J., and C. H. Graham. 2005. Niche conservatism: integrating evolution, ecology and conservation biology. Annu. Rev. Ecol. Evol. Syst. 36 : 519 539.
85. Wilmé, L., S. M. Goodman, and J. Ganzhorn. 2006. Biogeographic evolution of Madagascar's microendemic biota. Science 312 : 1063 1065.
86. Wilson, R., J. Heinrichs, J. Hentschel, S. R. Gradstein, and H. Schneider. 2007. Steady diversification of derived liverworts under Tertiary climatic fluctuations. Biol. Lett. 3 : 566 569.
87. de Wit, M. J. 2003. Madagascar: heads it's a continent, tails it's an island. Annu. Rev. Earth. Pl. Sc. 31 : 213 248.
88. Yoder, A. D., and M. D. Nowak. 2006. Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu. Rev. Ecol. Evol. Syst. 37 : 405 431.
89. Yoder, A. D., and Z. Yang. 2004. Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol. Ecol. 13 : 757 773.
90. Yoder, A. D., M. Cartmill, M. Ruivolo, K. Smith, and R. Vilgalys. 1996. Ancient single origin for Malagasy primates. Proc. Natl. Acad. Sci. USA 93 : 5122 5126.
91. Yoder, A. D., M. M. Burns, S. Zehr, T. Delefosse, G. Veron, S. M. Goodman, and J. J. Flynn. 2003. Single origin of Malagasy Carnivora from an African ancestor. Nature 421 : 734 737.
92. Yuan, Y.-M., S. Wohlhauser, M. Möller, J. Klackenberg, M. W. Callmander, and P. Küpfer. 2005. Phylogeny and biogeography of Exacum (Gentianaceae): a disjunctive distribution in the Indian Ocean Basin resulted from long distance dispersal and extensive radiation. Syst. Biol. 54 : 21 34.