The origins and diversification of C4 grasses and savanna-adapted ungulates

Global Change Biology

Volumn 15, Issue 10, 2009, Pages 2397-2417

  Bouchenak Khelladi, Yanis ^a,b   Verboom, G Anthony ^b   Hodkinson, Trevor R ^a   Salamin, Nicolas ^c   Francois, Olivier ^d   Ní Chonghaile, Grainne ^a   Savolainen, Vincent ^e,f  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d LABORATOIRE TIMC IMAG   (France)

^e ROYAL BOTANIC GARDENS   (United Kingdom)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

C4 ecosystems; CO2 level; Coevolution; Evolutionary history; Grasses; Grazing; Hypsodonty; Phylogenetic trees; Silica density; Ungulates

Indexed keywords

CARBON DIOXIDE; CARBON FIXATION; FOSSIL RECORD; GRAZING PRESSURE; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; SAVANNA; TROPICAL ENVIRONMENT; UNGULATE;

ANIMALIA; CHLORIDOIDEAE; POACEAE; UNGULATA;

EID: 70149113944     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2009.01860.x     Document Type: Article

References (87)

1. Aliscioni SS, Giussani LM, Zuloaga FO, Kellogg EA (2003) A molecular phyloTeny of Panicum (Poaceae: Paniceae): tests of monophyly and phylogenetic placement within the Panicoideae. American Journal of Botany, 90, 796-821.
2. Barker NPE, Harley E, Linder HP (1995) Phylogeny of Poaceae based on rbcL sequences. Systematic Botany, 20, 423-435.
3. Beerling DJ, Osborne CP (2006) The origin of the savanna biome. Global Change Biology, 12, 2023-2031.
4. Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. The American Naturalist, 127, 870-892.
5. Bininda-Emonds ORP, Cardillo M, Jones KE et al. (2007) The delayed rise of present-day mammals. Nature, 446, 507-512.
6. 2 and fire in promoting the spread of grasslands and savannas. Global Change Biology, 9, 973-982.
7. Bortolussi N, Durand E, Blum MGB, Francois O (2006) ApTreeshape: A statistical analysis of phylogenetic treeshape. Bioinformatics, 22, 363-364.
8. Bouchenak-Khelladi Y (2007) Grass evolution and diversification: A phylogenetic approach. PhD thesis, Trinity College Dublin.
9. Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, van der Bank M, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): Progress towards complete tribal and generic level sampling. Molecular Phylogenetics and Evolution, 47, 488-505.
10. Bremer K (2002) Gondwana evolution of the grass alliance of families (Poales). Evolution, 56, 1374-1387.
11. Bro-Jorgensen J (2007) The intensity of sexual selection predicts weapon size in male bovids. Evolution, 61, 1316-1326.
12. Cerling TE, Harris JM, Macfadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/ Pliocene boundary. Nature, 389, 153-158.
13. Chapman GP (1996) From extinct to present-day grasses. In: The Biology of Grasses (ed. Chapman GP), pp. 112-123. CAB International, Oxon, UK.
14. Chase MW, Hills DM (1991) Silica gel: An ideal material for field preservation of leaf samples for DNA studies. Taxon, 40, 215-220.
15. 4 photosynthesis in grasses. Current Biology, 18, 37-43.
16. Clark LG, Zhang W, Wendel JF (1995) A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Systematic Botany, 20, 436-460.
17. Clayton WD, Renvoize SA (1986) Genera Graminum, Grasses of the World. Her majesty's stationery office (ed.), London, UK.
18. Coughenour MB (1985) Graminoid responses to grazing by large herbivores: adaptations, exaptations, and interacting processes. Annals of the Missouri Botanical Gardens, 72, 852-863.
19. Crepet WL, Feldman GD (1991) The earliest remains of grasses in the fossil record. American Journal of Botany, 78, 1010-1014.
20. Doyle JJ, Doyle JL (1987) A rapid isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin, 19, 65-66.
21. Drinnan AN, Crane PR (1994) A synopsis of medullosan pollen organs from the Middle Pennsylvanian Mazon Creek flora of northeastern Illinois, USA. Review of Paleobotany and Palynology, 80, 235-257.
22. Dugas DP, Retallack GJ (1993) Middle Miocene fossil grasses from Fort Ternan, Kenya. Journal of Paleontology, 67, 113-128.
23. 4 grasses. Ecology Letters, 11, 266-276.
24. Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics, 24, 411-439.
25. Ellis RP (1990) Tannin-like substances in grass leaves. Memoirs of the Botanical Survey of South Africa, Pretoria, South Africa.
26. GPWG (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Annals of the Missouri Botanical Gardens, 88, 373-457.
27. Harding EF (1971) The probabilities of rooted tree-shapes generated by random bifunction. Advances in Applied Probability, 3, 44-77.
28. Harris TE (1964) The Theory of Branching Process. Springer-Verlag, Berlin.
29. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160-174.
30. Hassanin A, Douzery EJP (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution, 13, 227-243.
31. Hassanin A, Douzery EJP (2003) Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Systematic Biology, 52, 206-228.
32. 4-dicarboxylic acid. Biochemistry Journal, 125, 425-432.
33. 4 photosynthesis: A unique blend of modified biochemistry, anatomy and ultrastructure. Biochemica et Biophysica Acta, 895, 81-106.
34. Hattersley PW, Watson L (1975) Anatomical parameters for predicting photosynthetic pathways in grass leaves. Phytomorphology, 25, 325-333.
35. Hattersley PW, Watson L (1992) Diversification of photosynthesis. In: Grass Evolution and Domestication (ed. Chapman GP), pp. 38-116. Cambridge University Press, Cambridge, UK.
36. 2 records. Paleooceanography, 23.
37. 2: Natural Variations Archean to Present (eds Sundquist ET, Broecker WS), pp. 419-442. American Geophysical Union, Washington, DC.
38. Hodkinson TR, Salamin N, Chase MW, Bouchenak-Khelladi Y, Renvoize SA, Savolainen V (2007a) Large trees, supertrees and diversification of the grass family. Aliso, 23, 248-258.
39. Hodkinson TR, Savolainen V, Jacobs SWL, Bouchenak-Khelladi Y, Kinney MS, Salamin N (2007b) Supersizing: Progress in documenting and understanding grass species richness. In: Reconstructing the Tree of Life: Taxonomy and Systematics of Species Rich Taxa (eds Hodkinson TR, Parnell JAN), pp. 279-298. Taylor and Francis, CRC Press, Boca Raton, FL, USA.
40. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic tree. Bioinformatics, 17, 754-755.
41. Janis CM (1993) Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecological Systematics, 24, 467-500.
42. Janis CM, Damuth J, Theodor JM (2002) The origins and evolution of the North American grassland biome: The story from the hoofed mammals. Palaeogeography, Palaeoclimatology, Palaeoecology, 177, 183-198.
43. Jernvall J, Fortelius M (2002) Common mammals drive the evolutionary increase of hypsodonty in the Neogene. Nature, 417, 538-540.
44. Jernvall J, Hunter JP, Fortelius M (1996) Molar tooth diversity, disparity, and ecology in Cenozoic Ungulate radiations. Science, 274, 1489-1492.
45. Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ (2008) The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. American Journal of Botany, 95, 521-530.
46. 4 grasslands. Ecology Letters, 8, 683-690.
47. Kellogg EA (2000) The grasses: A case study in macroevolution. Review of Ecology and Systematics, 31, 217-238.
48. Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiology, 125, 1198-1205.
49. Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Science USA, 78, 454-458.
50. Kürschner WM, Kvacek Z, Dilcher DL (2008) The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proceedings of the National Academy of Science USA, 105, 449-453.
51. Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character. Systematic Biology, 50, 913-925.
52. Macfadden BJ, Cerling TE (1994) Fossil horses, carbon isotopes and global change. Trends in Ecology and Evolution, 9, 481-486.
53. Maddison DR, Maddison WP (2005) MacClade 4. Version 4.08 for OSX. Sinauer Associates, Sunderland, MA.
54. Maddison WP, Maddison DR (2006) Mesquite: A modular system for evolutionary analysis. Version 1.12. http://mesquiteproject.org
55. Massey FP, Hartley SE (2006) Experimental demonstration of the antiherbivore effects of silica in grasses: Impacts on foliage digestibility and vole growth rates. Proceedings of the Royal Society B-Biological Sciences, 273, 2299-2304.
56. Matthee CA, Davis SK (2001) Molecular insights into the evolution of the family Bovidae: A nuclear DNA study. Molecular Biology and Evolution, 18, 1220-1230.
57. Moore BR, Chan KMA, Donoghue MJ (2004) Detecting diversification rate variation in supertrees. In: Phylogenetic Supertrees: Combining Information to Reveal the Trees of Life (ed. Bininda-Emonds ORP), pp. 487-533. Kluwer Academic, Dordrecht, the Netherlands.
58. Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA (2006) The animal diversity web. Accessed December 2007 at http://animaldiversity.org
59. Nelder J, Wedderburn R (1972) Generalized linear models. Journal of the Royal Statistical Society Series A, 135, 370-384.
60. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology, 53, 47-67.
61. 4 plants. Philosophical Transactions of the Royal Society B, 361, 173-194.
62. Pagani M, Zachos J, Freeman KH, Bohaty S, Tipple B (2005) Marked change in atmospheric carbon dioxide concentrations during the Oligocene. Science, 309, 600-603.
63. Pagel M (1999b) The maximum likelihood approach for reconstructing ancestral character sates of discrete characters on phylogenies. Systematic Biology, 48, 612-622.
64. Paradis E, Claude J (2002) Comparative data and GEE. Journal of Theoretical Biology, 218, 175-185.
65. Piperno DR (2006) Phytoliths: A Comprehensive Guide for Archeologists and Paleoecologists. AltaMira Press, Lanham, MD, USA.
66. Posada D, Crandall K (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics, 14, 817-818.
67. Prasad V, Stromberg CAE, Alimohammadian H, Shani A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science, 310, 1177-1180.
68. Purvis A (1995) A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London B, 348, 405-421.
69. 4 photosynthesis: Convergence upon convergence upon... Current Biology, 17, 776-778.
70. 4 photosynthesis: Differentiating causation and coincidence. Current Biology, 18, 167-168.
71. Roodt-Wilding R, Spies JJ (2006) Phylogenetic relationships in southern African chloridoid grasses (Poaceae) based on nuclear and chloroplast sequence data. Systematics and Biodiversity, 4, 401-415.
72. 4 photosynthetic syndrome. Plant Biology, 3, 202-213.
73. 4 photosynthesis. New Phytologist, 161, 341-370.
74. 4 Plant Biology. Academic Press, San Diego, CA.
75. Sanchez-Ken JG, Clark LG, Kellogg EA, Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Systematic Botany, 32, 71-80.
76. 4 photosynthesis in the grass family. American Journal of Botany, 83, 1458-1470.
77. Stebbins GL, Crampton B (1961) A suggested revision of the grass genera of temperate North America. In: Recent Advances in Botany (IXth International Botanical Congress, Montreal, Canada), Vol. 1. Toronto University Press, Toronto, Canada.
78. Stromberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Science USA, 102, 11980-11984.
79. Stromberg CAE (2006) Evolution of hypsodonty in equids: Testing a hypothesis of adaptation. Paleobiology, 32, 236-258.
80. Sungkaew S, Stapleton CMA, Salamin N, Hodkinson TR (2009) Non-monophyly of tAe woody bamboos (Bambuseae: Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae s.s. Journal of Plant Research, 122, 95-108.
81. 4 grasses. American Journal of Botany, 87, 412-417.
82. Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology, 51, 689-702.
83. 4 photosynthesis. Annual Reviews of Earth and Planetary Sciences, 35, 435-461.
84. 4 photosynthesis. Global Change Biology, 14, 1-15.
85. Watson L, Dallwitz MJ (1992) The Grass Genera of the World. CAB International, Wallingford, UK.
86. Yang ZH (1994) Maximum-likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. Journal of Molecular Evolution, 39, 306-314.
87. Zazzo A, Bocherens H, Brunet M et al. (2000) Herbivore paleo-diet and paleo-environmental changes in Chad during the Pliocene using stable isotope ratios of tooth enamel carbonate. Paleobiology, 26, 294-309.