Abstract
Fire may have been a crucial component in the evolution of the Cape flora of South Africa, a region characterized by outstanding levels of species richness and endemism. However, there is, to date, no critical assessment of the age of the modern fire regime in this biome. Here, we exploit the presence of two obligate post-fire flowering clades in the orchid genus Disa, in conjunction with a robust, well-sampled and dated molecular phylogeny, to estimate the age by which fire must have been present. Our results indicate that summer drought (winter rainfall), the fire regime and the fynbos vegetation are several million years older than currently suggested. Summer drought and the fynbos vegetation are estimated to date back to at least the Early Miocene (ca 19.5 Ma). The current fire regime may have been established during a period of global cooling that followed the mid-Miocene Climatic Optimum (ca 15 Ma), which led to the expansion of open habitats and increased aridification. The first appearance of Disa species in the grassland biome, as well as in the subalpine habitat, is in striking agreement with reliable geological and palaeontological evidence of the age of these ecosystems, thus corroborating the efficacy of our methods. These results change our understanding of the historical mechanisms underlying botanical evolution in southern Africa, and confirm the potential of using molecular phylogenies to date events for which other information is lacking or inconclusive.
References
- 1
Bowman D. M. J. S., 2009 Fire in the Earth system. Science 324, 481–484.doi:10.1126/science.1163886 (doi:10.1126/science.1163886). Crossref, PubMed, Web of Science, Google Scholar - 2
Simon M. F., Grether R., de Queiroz L. P., Skema C., Pennington R. T.& Hughes C. E. . 2009 Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc. Natl Acad. Sci. USA 106, 20359–20364.doi:10.1073/pnas.0903410106 (doi:10.1073/pnas.0903410106). Crossref, PubMed, Web of Science, Google Scholar - 3
Bond W. J.& Keeley J. E. . 2005 Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol. Evol. 20, 387–394.doi:10.1016/j.tree.2005.04.025 (doi:10.1016/j.tree.2005.04.025). Crossref, PubMed, Web of Science, Google Scholar - 4
Bond W. J., Woodward F. I.& Midgley G. F. . 2005 The global distribution of ecosystems in a world without fire. New Phytol. 165, 525–538.doi:10.1111/j.1469-8137.2004.01252.x (doi:10.1111/j.1469-8137.2004.01252.x). Crossref, PubMed, Web of Science, Google Scholar - 5
Scott A. C. . 2000 The pre-quaternary history of fire. Paleogeogr. Paleoclimatol. Paleoecol. 164, 281–329.doi:10.1016/S0031-0182(00)00192-9 (doi:10.1016/S0031-0182(00)00192-9). Crossref, Web of Science, Google Scholar - 6
Scott A. C.& Glasspool I. J. . 2006 The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. Proc. Natl Acad. Sci. USA 103, 10861–10865.doi:10.1073/pnas.0604090103 (doi:10.1073/pnas.0604090103). Crossref, PubMed, Web of Science, Google Scholar - 7
van der Hammen T.& Hooghiemstra H. . 2000 Neogene and quaternary history of vegetation, climate, and plant diversity in Amazonia. Quat. Sci. Rev. 19, 725–742.doi:10.1016/S0277-3791(99)00024-4 (doi:10.1016/S0277-3791(99)00024-4). Crossref, Web of Science, Google Scholar - 8
Jacobs B. . 2004 Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. Phil. Trans. R. Soc. B 359, 1573–1583.doi:10.1098/rstb.2004.1533 (doi:10.1098/rstb.2004.1533). Link, Web of Science, Google Scholar - 9
Jacobs B. F.& Herendeen P. S. . 2004 Eocene dry climate and woodland vegetation in tropical Africa reconstructed from fossil leaves from northern Tanzania. Paleogeogr. Paleoclimatol. Paleoecol. 213, 115–123. Crossref, Web of Science, Google Scholar - 10
Diester-Haass L., Meyers A. P.& Rothe P. . 1992 The Benguela current and associated upwelling on the southwest African margin: a synthesis of the Neogene-Quaternary sedimentary record at DSDP sites 362 and 532. Upwelling systems: evolution since the Early Miocene vol. 64 (eds, Summerhayes C. P., Prell W. L.& Emeis K. C. ), pp. 331–342. London, UK: Geological Society Special Publication. Google Scholar - 11
Zachos J., Pagani M., Sloan L., Thomas E.& Billups K. . 2001 Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693.doi:10.1126/science.1059412 (doi:10.1126/science.1059412). Crossref, PubMed, Web of Science, Google Scholar - 12
Bobe R. . 2006 The evolution of arid ecosystems in eastern Africa. J. Arid Environ. 66, 564–584.doi:10.1016/j.jaridenv.2006.01.010 (doi:10.1016/j.jaridenv.2006.01.010). Crossref, Web of Science, Google Scholar - 13
Linder H. P. . 2003 The radiation of the Cape flora, southern Africa. Biol. Rev. 78, 597–638.doi:10.1017/S1464793103006171 (doi:10.1017/S1464793103006171). Crossref, PubMed, Web of Science, Google Scholar - 14
Goldblatt P.& Manning J. . 2000 Cape plants. A conspectus of the Cape flora of South Africa. Strelitzia Cape Town, South Africa: National Botanical Institute. Google Scholar - 15
Goldblatt P., Manning J. C.& Snijman D. A. . 2005 Cape plants: corrections and additions to the flora. 1. Bothalia 35, 35–46. Crossref, Web of Science, Google Scholar - 16
Kier G., Kreft H., Lee T. M., Jetz W., Ibisch P. L., Nowicki C., Mutke J.& Barthlott W. . 2009 A global assessment of endemism and species richness across island and mainland regions. Proc. Natl Acad. Sci. USA 106, 9322–9327.doi:10.1073/pnas.0810306106 (doi:10.1073/pnas.0810306106). Crossref, PubMed, Web of Science, Google Scholar - 17
Rebelo A. G., Boucher C., Helme N. A., Mucina L.& Rutherford M. C. . 2006 Fynbos biome. The vegetation of South Africa, Lesotho and Swaziland, Strelitzia, vol. 19 (eds, Mucina L.& Rutherford M. C. ), pp. 52–219. Pretoria, South Africa: South African National Biodiversity Institute. Google Scholar - 18
Goldblatt P. . 1978 An analysis of the flora of southern Africa: its characteristics, relationships, and orgins. Ann. Mo. Bot. Gard. 65, 369–436.doi:10.2307/2398858 (doi:10.2307/2398858). Crossref, Web of Science, Google Scholar - 19
Richardson J. E., Weitz F. M., Fay M. F., Cronk Q. C. B., Linder H. P., Reeves G.& Chase M. W. . 2001 Rapid and recent origin of species richness in the Cape flora of South Africa. Nature 412, 181–183.doi:10.1038/35084067 (doi:10.1038/35084067). Crossref, PubMed, Web of Science, Google Scholar - 20
Klak C., Reeves G.& Hedderson T. . 2004 Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427, 63–65.doi:10.1038/nature02243 (doi:10.1038/nature02243). Crossref, PubMed, Web of Science, Google Scholar - 21
Goldblatt P., Savolainen V., Porteous O., Sostaric I., Powell M., Reeves G., Manning J. C., Barraclough T. G.& Chase M. W. . 2002 Radiation in the Cape flora and the phylogeny of peacock irises Moraea (Iridaceae) based on four plastid DNA regions. Mol. Phylogenet. Evol. 25, 341–360.doi:10.1016/S1055-7903(02)00235-X (doi:10.1016/S1055-7903(02)00235-X). Crossref, PubMed, Web of Science, Google Scholar - 22
Bakker F. T., Culham A., Marais E. M.& Gibby M. . 2005 Nested radiation in Cape Pelargonium. Plant species-level systematics: new perspectives on pattern and process, Regnum Vegetabile, vol. 143 (eds, Bakker F. T., Chatrou L. W., Barbara G.& Pelser P. B. ), pp. 75–100. Ruggel, Liechtenstein: A.R.G. Gantner Verlag. Google Scholar - 23
Kreft H.& Jetz W. . 2007 Global patterns and determinants of vascular plant diversity. Proc. Natl Acad. Sci. USA 104, 5925–5930.doi:10.1073/pnas.0608361104 (doi:10.1073/pnas.0608361104). Crossref, PubMed, Web of Science, Google Scholar - 24
- 25
Verboom G. A., 2009 Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Mol. Phylogenet. Evol. 51, 44–53.doi:10.1016/j.ympev.2008.01.037 (doi:10.1016/j.ympev.2008.01.037). Crossref, PubMed, Web of Science, Google Scholar - 26
Linder H. P. . 2008 Plant species radiations: where, when, why? Phil. Trans. R. Soc. B 363, 3097–3105.doi:10.1098/rstb.2008.0075 (doi:10.1098/rstb.2008.0075). Link, Web of Science, Google Scholar - 27
Linder H. P. . 2005 Evolution of diversity: the Cape flora. Trends Plant Sci. 10, 536–541. Crossref, PubMed, Web of Science, Google Scholar - 28
Cowling R. M., Proches S.& Partridge T. C. . 2009 Explaining the uniqueness of the Cape flora: incorporating geomorphic evolution as a factor for explaining its diversification. Mol. Phylogenet. Evol. 51, 64–74.doi:10.1016/j.ympev.2008.05.034 (doi:10.1016/j.ympev.2008.05.034). Crossref, PubMed, Web of Science, Google Scholar - 29
Bytebier B., Bellstedt D. U.& Linder P. H. . 2008 A new phylogeny-based sectional classification for the large African orchid genus Disa. Taxon 57, 1233–1251. Crossref, Web of Science, Google Scholar - 30
Linder H. P.& Kurzweil H. . 1999 Orchids of southern Africa. Rotterdam/Brookfield: A.A. Balkema. Google Scholar - 31
Bytebier B., Bellstedt D. U.& Linder P. H. . 2007 A molecular phylogeny for the large African orchid genus Disa. Mol. Phylogenet. Evol. 43, 75–90.doi:10.1016/j.ympev.2006.08.014 (doi:10.1016/j.ympev.2006.08.014). Crossref, PubMed, Web of Science, Google Scholar - 32
Gustafsson A. L., Verola C.& Antonelli A. . 2010 Reassessing the temporal evolution of orchids with new fossils and a Bayesian relaxed clock, with implications for the diversification of the rare South American genus Hoffmannseggella (Orchidaceae: Epidendroideae). BMC Evol. Biol. 10, 177.doi:10.1186/1471-2148-10-177 (doi:10.1186/1471-2148-10-177). Crossref, PubMed, Web of Science, Google Scholar - 33
Sanderson M. J. . 2002 Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109. Crossref, PubMed, Web of Science, Google Scholar - 34
Drummond A.& Rambaut A. . 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.doi:10.1186/1471-2148-7-214 (doi:10.1186/1471-2148-7-214). Crossref, PubMed, Web of Science, Google Scholar - 35
Ramirez S. R., Gravendeel B., Singer R. B., Marshall C. R.& Pierce N. E. . 2007 Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448, 1042–1045.doi:10.1038/nature06039 (doi:10.1038/nature06039). Crossref, PubMed, Web of Science, Google Scholar - 36
Conran J. G., Bannister J. M.& Lee D. E. . 2009 Earliest orchid macrofossils: early Miocene Dendrobium and Earina (Orchidaceae: Epidendroideae) from New Zealand. Am. J. Bot. 96, 466–474.doi:10.3732/ajb.0800269 (doi:10.3732/ajb.0800269). Crossref, PubMed, Web of Science, Google Scholar - 37
Doyle J., Endress P.& Upchurch G. . 2008 Early Cretaceous monocots: a phylogenetic evaluation. Acta Musei Nation. Pragae, Ser. B, Hist. Nat. 64, 59–87. Google Scholar - 38
Hardy C. R.& Linder H. P. . 2005 Intraspecific variability and timing in ancestral ecology reconstruction: a test case from the Cape flora. Syst. Biol. 54, 299–316.doi:10.1080/10635150590923317 (doi:10.1080/10635150590923317). Crossref, PubMed, Web of Science, Google Scholar - 39
Maddison W. P.& Maddison D. R. . 2009 Mesquite: a modular system for evolutionary analysis. Version 2.6. See http://mesquiteproject.org. Google Scholar - 40
Frajman B., Eggens F.& Oxelman B. . 2009 Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae)—a multigene phylogenetic approach with relative dating. Syst. Biol. 58, 328–345.doi:10.1093/sysbio/syp030 (doi:10.1093/sysbio/syp030). Crossref, PubMed, Web of Science, Google Scholar - 41
Levyns M. R. . 1964 Migrations and origin of the Cape flora. Trans. R. Soc. S. Afr. 37, 85–107. Crossref, Google Scholar - 42
Axelrod D. I.& Raven P. H. . 1978 Late Cretaceous and Tertiary vegetation history of Africa. Biogeography and ecology of southern Africa, Monographiae Biologicae, vol. 31 (ed.& Werger M. J. A. ), pp. 77–130. Hague, The Netherlands: Dr. W. Junk bv Publishers. Google Scholar - 43
Linder H. P., Meadows M. E.& Cowling R. M. . 1992 History of the Cape flora. The ecology of fynbos, nutrients, fire and diversity (ed.& Cowling R. M. ), pp. 114–134. Oxford, UK: Oxford University Press. Google Scholar - 44
Goldblatt P.& Manning J. C. . 2002 Plant diversity of the Cape region of southern Africa. Ann. Mo. Bot. Gard. 89, 281–302.doi:10.2307/3298566 (doi:10.2307/3298566). Crossref, Web of Science, Google Scholar - 45
Zachos J. C., Dickens G. R.& Zeebe R. E. . 2008 An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451, 279–283.doi:10.1038/nature06588 (doi:10.1038/nature06588). Crossref, PubMed, Web of Science, Google Scholar - 46
Sauquet H., Weston P. H., Barker N. P., Anderson C. L., Cantrill D. J.& Savolainen V. . 2009 Using fossils and molecular data to reveal the origins of the Cape proteas (subfamily Proteoideae). Mol. Phylogenet. Evol. 51, 31–43.doi:10.1016/j.ympev.2008.12.013 (doi:10.1016/j.ympev.2008.12.013). Crossref, PubMed, Web of Science, Google Scholar - 47
Forest F., Nanni I., Chase M. W., Crane P. R.& Hawkins J. A. . 2007 Diversification of a large genus in a continental biodiversity hotspot: temporal and spatial origin of Muraltia (Polygalaceae) in the Cape of South Africa. Mol. Phylogenet. Evol. 43, 60–74.doi:10.1016/j.ympev.2006.08.017 (doi:10.1016/j.ympev.2006.08.017). Crossref, PubMed, Web of Science, Google Scholar - 48
Quint M.& Claßen-Bockhoff R. . 2008 Ancient or recent? Insights into the temporal evolution of the Bruniaceae. Org. Divers. Evol. 8, 293–304.doi:10.1016/j.ode.2008.03.001 (doi:10.1016/j.ode.2008.03.001). Crossref, Web of Science, Google Scholar - 49
Edwards D.& Hawkins J. A. . 2007 Are Cape floral clades the same age? Contemporaneous origins of two lineages in the genistoids s.l. (Fabaceae). Mol. Phylogenet. Evol. 45, 952–970. Crossref, PubMed, Web of Science, Google Scholar - 50
Scholtz A. . 1985 The palynology of the upper lacustrine sediments of the Arnot Pipe, Banke, Namaqualand. Ann. S. African Mus. 95, 1–109. Google Scholar - 51
Thiergart F., Frantz U.& Raukopf K. . 1963 Palynologische Untersuchungen von Tertiärkohlen und einer oberflächen Probe nähe Knysna, Südafrika. Advancing Front. Plant Sci. 4, 151–178. Google Scholar - 52
Coetzee J. A. . 1983 Intimations of the tertiary vegetation of southern Africa. Bothalia 14, 345–354. Crossref, Google Scholar - 53
Thwaites R. N.& Jacobs E. O. . 1989 The Cenozoic history of the coastal landscape of the southern Cape province, South Africa: a review. Quat. Sci. Rev. 8, 283–293.doi:10.1016/0277-3791(89)90043-7 (doi:10.1016/0277-3791(89)90043-7). Crossref, Web of Science, Google Scholar - 54
Siesser W. G. . 1978 Aridification of the Namib Desert; evidence from ocean cores. Antartic glacial history and world paleoenvironments (ed.& Van Zinderen-Bakker E. M. ), pp. 105–113. Rotterdam, The Netherlands: A.A. Balkema. Google Scholar - 55
Siesser W. G. . 1980 Late Miocene origin of the Benguela upwelling system off northern Namibia. Science 208, 283–285.doi:10.1126/science.208.4441.283 (doi:10.1126/science.208.4441.283). Crossref, PubMed, Web of Science, Google Scholar - 56
Diester-Haass L., Meyers P. A.& Vidal L. . 2002 The late Miocene onset of high productivity in the Benguela Current upwelling system as part of a global pattern. Mar. Geol. 180, 87–103.doi:10.1016/S0025-3227(01)00207-9 (doi:10.1016/S0025-3227(01)00207-9). Crossref, Web of Science, Google Scholar - 57
Keeley J. E.& Rundel P. W. . 2005 Fire and the Miocene expansion of C4 grasslands. Ecol. Lett. 8, 683–690.doi:10.1111/j.1461-0248.2005.00767.x (doi:10.1111/j.1461-0248.2005.00767.x). Crossref, Web of Science, Google Scholar - 58
Gill A. M.& Catling P. C. . 2002 Fire regimes and biodiversity of forested landscapes of southern Australia. Flammable Australia. The fire regimes and biodiversity of a continent (eds, Bradstock R. A., Williams J. E.& Gill A. M. ), pp. 351–369. Cambridge, UK: Cambridge University Press. Google Scholar - 59
Kershaw A. P., Clark J. S., Gill A. M.& D'Costa D. M. . 2002 A history of fire in Australia. Flammable Australia. The fire regimes and biodiversity of a continent (eds, Bradstock R. A., Williams J. E.& Gill M. A. ), pp. 3–23. Cambridge, UK: Cambridge University Press. Google Scholar - 60
Hill R. S. . 2004 Origins of the southeastern Australian vegetation. Phil. Trans. R. Soc. Lond. B 359, 1537–1549.doi:10.1098/rstb.2004.1526 (doi:10.1098/rstb.2004.1526). Link, Web of Science, Google Scholar - 61
Atahan P., Dodson J. R.& Itzstein-Davey F. . 2004 A fine-resolution Pliocene pollen and charcoal record from Yallalie, south-western Australia. J. Biogeogr. 31, 199–205. Crossref, Web of Science, Google Scholar - 62
Peterson A. T., Soberón J.& Sánchez-Cordero V. . 1999 Conservatism of ecological niches in evolutionary time. Science 285, 1265–1267.doi:10.1126/science.285.5431.1265 (doi:10.1126/science.285.5431.1265). Crossref, PubMed, Web of Science, Google Scholar - 63
Patterson T. B.& Givnish T. J. . 2002 Phylogeny, concerted convergence, and phylogenetic niche conservatism in the core Liliales: insights from rbcL and ndhF sequence data. Evolution 56, 233–252. Crossref, PubMed, Web of Science, Google Scholar - 64
Ackerly D. D. . 2003 Community assembly, niche conservatism, and adaptive evolution in changing environments. Int. J. Plant Sci. 164, S165.doi:10.1086/368401 (doi:10.1086/368401). Crossref, Web of Science, Google Scholar - 65
Svenning C. . 2003 Deterministic Plio-Pleistocene extinctions in the European cool-temperate tree flora. Ecol. Lett. 6, 646–653.doi:10.1046/j.1461-0248.2003.00477.x (doi:10.1046/j.1461-0248.2003.00477.x). Crossref, Web of Science, Google Scholar - 66
Crisp M. D., 2009 Phylogenetic biome conservatism on a global scale. Nature 458, 754–756.doi:10.1038/nature07764 (doi:10.1038/nature07764). Crossref, PubMed, Web of Science, Google Scholar - 67
Bouchenak-Khelladi Y., Verboom G. A., Savolainen V.& Hodkinson T. R. . 2010 Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot. J. Linn. Soc. 162, 543–557.doi:10.1111/j.1095-8339.2010.01041.x (doi:10.1111/j.1095-8339.2010.01041.x). Crossref, Web of Science, Google Scholar - 68
Adegoke O. S., Jan du Chene R. E., Agumane A. E.& Ajayi P. O. . 1978 Palynology and age of the Keri-Keri Formation, Nigeria. Revista Esp. Micropaleontol. 10, 267–282. Google Scholar - 69
Jacobs B. F., Kingston J. D.& Jacobs L. L. . 1999 The origin of grass-dominated ecosystems. Ann. Mo. Bot. Gard. 86, 590–643.doi:10.2307/2666186 (doi:10.2307/2666186). Crossref, Web of Science, Google Scholar - 70
Morley R. J.& Richards K. . 1993 Gramineae cuticle—a key indicator of late Cenozoic climatic-change in the Niger Delta. Rev. Palaeobot. Palynol. 77, 119–127.doi:10.1016/0034-6667(93)90060-8 (doi:10.1016/0034-6667(93)90060-8). Crossref, Web of Science, Google Scholar - 71
Retallack G. J. . 1992 Middle Miocene fossil plants from Fort Ternan (Kenya) and evolution of African grasslands. Paleobiology 18, 383–400. Crossref, Web of Science, Google Scholar - 72
Dugas D. P.& Retallack G. J. . 1993 Middle Miocene fossil grasses from Fort Ternan, Kenya. J. Paleontol. 67, 113–128. Crossref, Web of Science, Google Scholar - 73
Antonelli A., Verola C., Parisod C.& Gustafsson A. L. . 2010 Climate cooling promoted the expansion and radiation of a threatened group of South American orchids (Epidendroideae: Laeliinae). Biol. J. Linn. Soc. 100, 597–607.doi:10.1111/j.1095-8312.2010.01438.x (doi:10.1111/j.1095-8312.2010.01438.x). Crossref, Web of Science, Google Scholar - 74
Crisp M. D., Isagi Y., Kato Y., Cook L. G.& Bowman D. M. J. S. . 2010 Livistona palms in Australia: Ancient relics or opportunistic immigrants? Mol. Phylogenet. Evol. 54, 512–523.doi:10.1016/j.ympev.2009.09.020 (doi:10.1016/j.ympev.2009.09.020). Crossref, PubMed, Web of Science, Google Scholar - 75
Partridge T. C., Wood B. A.& deMenocal P. B. . 1995 The influence of global climatic change and regional uplift on large-mammalian evolution in east and southern Africa. Paleoclimate and evolution, with emphasis on human origins (eds, Vrba E. S., Denton G. H., Partridge T. C.& Burckle L. H. ), pp. 331–355. New Haven, CT: Yale University Press. Google Scholar - 76
McCarthy T.& Rubidge B. . 2005 The story of earth and life. A southern African perspective on a 4.6-billion-year journey. Cape Town, South Africa: Struik Publishers. Google Scholar - 77
Gradstein F. M.& Ogg J. G. . 2004 Geologic Time Scale 2004: why, how, and where next!. Lethaia 37, 175–181.doi:10.1080/00241160410006483 (doi:10.1080/00241160410006483). Crossref, Web of Science, Google Scholar