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Plant Systematics and Evolution

, Volume 298, Issue 1, pp 221–227 | Cite as

Diversification rates in the Australasian endemic grass Austrostipa: 15 million years of constant evolution

  • Anna E. SymeEmail author
Original Article

Abstract

Patterns seen in other Australian flora have led to hypotheses that early Miocene shifts in climate drove rapid radiation of major taxonomic groups such as Eucalyptus. Little is known about absolute dates and rates for Australian monocots, particularly grasses. I tested this early Miocene radiation hypothesis for Australian grasses using a calibrated phylogeny of the endemic stipoid genus Austrostipa and an analysis of diversification rates. The phylogeny was developed from a Bayesian likelihood analysis of the nuclear internal transcribed spacers region, and three calibration points were set based on fossil evidence. The results indicate that the genus arose in the early Miocene and underwent a species radiation, but the rate of diversification was not rapid compared to the current rate or to those of other taxa. Following an 8 million year period of fast molecular evolution but no taxonomic radiation, diversification rates have been constant for the past 15 million years. Comparable measures such as the gamma statistic can be used across taxa to make general conclusions about evolutionary rate constancy.

Keywords

Poaceae Stipeae Phylogeny Radiation Molecular evolution 

Notes

Acknowledgments

I thank the staff at the National Herbarium of Victoria, Australia, for providing the sequence data for Austrostipa specimens and Frank Udovicic for comments on the draft of this paper.

References

  1. Bendiksby M, Schumacher T, Gussarova G, Nais J, Mat-Salleh K, Sofiyanti N, Madulid D, Smith SA, Barkman T (2010) Elucidating the evolutionary history of the Southeast Asian, holoparasitic, giant-flowered Rafflesiaceae: Pliocene vicariance, morphological convergence and character displacement. Mol Phylogenet Evol 57(2):620–633. doi: 10.1016/j.ympev.2010.08.005 PubMedCrossRefGoogle Scholar
  2. Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, Mvd Bank, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47(2):488–505. doi: 10.1016/j.ympev.2008.01.035 PubMedCrossRefGoogle Scholar
  3. Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkinson TR (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot J Linn Soc 162(4):543–557. doi: 10.1111/j.1095-8339.2010.01041.x CrossRefGoogle Scholar
  4. Bremer K (2002) Gondwanan evolution of the grass alliance of families (Poales). Evolution 56(7):1374–1387PubMedGoogle Scholar
  5. 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(6647):153–158CrossRefGoogle Scholar
  6. Cialdella AM, Salariato DL, Aagesen L, Giussani LM, Zuloaga FO, Morrone O (2010) Phylogeny of new world Stipeae (Poaceae): an evaluation of the monophyly of Aciachne and Amelichloa. Cladistics 26:1–16. doi: 10.1111/j.1096-0031.2010.00310.x Google Scholar
  7. Crepet WL, Feldman GD (1991) The earliest remains of grasses in the fossil record. Am J Bot 78(7):1010–1014CrossRefGoogle Scholar
  8. Crisp MD, Cook LG (2009) Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 63(9):2257–2265. doi: 10.1111/j.1558-5646.2009.00728.x PubMedCrossRefGoogle Scholar
  9. Crisp M, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philos Trans R Soc Lond B 359:1551–1571CrossRefGoogle Scholar
  10. Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  11. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4(5):e88PubMedCrossRefGoogle Scholar
  12. Drummond A, Ho S, Rawlence N, Rambaut A (2007) A Rough Guide to BEAST 1.4. www.beast.bio.ed.ac.uk
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi: 10.1093/nar/gkh340 PubMedCrossRefGoogle Scholar
  14. Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc Nat Acad Sci 107(6):2532–2537. doi: 10.1073/pnas.0909672107 PubMedCrossRefGoogle Scholar
  15. Edwards EJ, Still CJ (2008) Climate, phylogeny and the ecological distribution of C4 grasses. Ecol Lett 11(3):266–276. doi: 10.1111/j.1461-0248.2007.01144.x PubMedCrossRefGoogle Scholar
  16. Forest F (2009) Calibrating the tree of life: fossils, molecules and evolutionary timescales. Ann Bot 104(5):789–794. doi: 10.1093/aob/mcp192 PubMedCrossRefGoogle Scholar
  17. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24(1):129–131. doi: 10.1093/bioinformatics/btm538 PubMedCrossRefGoogle Scholar
  18. Ho SYM (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. J Avian Biol 38(4):409–414. doi: 10.1111/j.0908-8857.2007.04168.x Google Scholar
  19. Ho SYW, Phillips MJ (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58(3):367–380. doi: 10.1093/sysbio/syp035 PubMedCrossRefGoogle Scholar
  20. Hsiao C, Jacobs SWL, Chatterton NJ, Asay KH (1999) A molecular phylogeny of the grass family (Poaceae) based on the sequences of nuclear ribosomal DNA (ITS). Aust Syst Bot 11:667–688CrossRefGoogle Scholar
  21. Jones R (1997) The biogeography of the grasses and lowland grasses of south-eastern Australia. Adv Nat Conserv 2:11–18Google Scholar
  22. Kay K, Whittall J, Hodges S (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol 6(1):36PubMedCrossRefGoogle Scholar
  23. Kellogg EA (2000) The grasses: a case study in macroevolution. Annu Rev Ecol Syst 31(1):217–238. doi: 10.1146/annurev.ecolsys.31.1.217 CrossRefGoogle Scholar
  24. Lancaster L (2010) Molecular evolutionary rates predict both extinction and speciation in temperate angiosperm lineages. BMC Evol Biol 10(1):162PubMedCrossRefGoogle Scholar
  25. Lawver LA, Gahagan LM (2003) Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeogr Palaeoclimatol Palaeoecol 198(1–2):11–37. doi: 10.1016/s0031-0182(03)00392-4 CrossRefGoogle Scholar
  26. Linder HP (1987) The evolutionary history of the Poales/Restionales—a hypothesis. Kew Bull 42:297–318CrossRefGoogle Scholar
  27. Linder HP (2008) Plant species radiations: where, when, why? Philos Trans R Soc B Biol Sci 363(1506):3097–3105. doi: 10.1098/rstb.2008.0075 CrossRefGoogle Scholar
  28. Macphail MK, Hill RS (2002) Paleobotany of the Poaceae. In: Mallett K (ed) Flora of Australia, vol 43. Australian Biological Resources Study/CSIRO Publishing, pp 37–70Google Scholar
  29. Magallon S, Castillo A (2009) Angiosperm diversification through time. Am J Bot 96(1):349–365. doi: 10.3732/ajb.0800060 PubMedCrossRefGoogle Scholar
  30. Martin HA (2006) Cenozoic climatic change and the development of the arid vegetation in Australia. J Arid Environ 66(3):533–563. doi: 10.1016/j.jaridenv.2006.01.009 CrossRefGoogle Scholar
  31. McCusker A (2002) Poaceae: family description. In: Mallett K (ed) Flora of Australia, vol 43. Australian Biological Resources Study/CSIRO Publishing, pp 1–3Google Scholar
  32. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290. doi: 10.1093/bioinformatics/btg412 PubMedCrossRefGoogle Scholar
  33. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818. doi: citeulike-article-id:2306418 PubMedCrossRefGoogle Scholar
  34. Prasad V, Stromberg CAE, Alimohammadian H, Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers.(Reports). Science 310(5751):1177–1180PubMedCrossRefGoogle Scholar
  35. Prothero DR (1994) The late Eocene–Oligocene extinctions. Annu Rev Earth Planet Sci 22(1):145–165. doi: 10.1146/annurev.ea.22.050194.001045 CrossRefGoogle Scholar
  36. Pybus OG, Harvey PH (2000) Testing macro-evolutionary models using incomplete molecular phylogenies. Proc Biol Sci 267(1459):2267–2272PubMedCrossRefGoogle Scholar
  37. Rambaut A (2009) FigTree version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree
  38. Rambaut A, Drummond A (2007) TRACER v1.4, Available from http://beast.bio.ed.ac.uk/Tracer
  39. Romaschenko K, Peterson PM, Soreng RJ, Garcia-Jacas N, Susanna A (2010) Phylogenetics of Stipeae (Poaceae: Pooidae) based on plastid and nuclear DNA sequences. In: Seberg O, Petersen G, Barfod A, Davis J (eds) Diversity, phylogeny and evolution in the monocotyledons. Aarhus University Press, AarhusGoogle Scholar
  40. Sandve SR, Fjellheim S (2010) Did gene family expansions during the Eocene–Oligocene boundary climate cooling play a role in Pooidae adaptation to cool climates? Mol Ecol 19:2075–2088PubMedCrossRefGoogle Scholar
  41. Schneider J, Winterfeld G, Hoffmann MH, Roser M (2011) Duthieeae, a new tribe of grasses (Poaceae) identified among the early diverging lineages of subfamily Pooideae: molecular phylogenetics, morphological delineation, cytogenetics and biogeography. Syst Biodivers 9(1):27–44. doi: 10.1080/14772000.2010.544339 CrossRefGoogle Scholar
  42. Stromberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proc Nat Acad Sci 102(34):11980–11984PubMedCrossRefGoogle Scholar
  43. Stromberg CAE, McInerney FA (2011) The Neogene transition from C3 to C4 grasslands in North America: assemblage analysis of fossil phytoliths. Paleobiology 37(1):50–71. doi: 10.1666/09067.1 CrossRefGoogle Scholar
  44. Thomasson JR (2005) Berriochloa gabeli and Berriochloa huletti (Gramineae: Stipeae), two new grass species from the late Miocene ash hollow formation of Nebraska and Kansas. J Paleontol 79(1):185–199CrossRefGoogle Scholar
  45. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14(12):2963–2977. doi: 10.1111/j.1365-2486.2008.01688.x CrossRefGoogle Scholar
  46. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science (New York, NY) 292(5517):686–693CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.National Herbarium of Victoria, Royal Botanic Gardens MelbourneSouth YarraAustralia

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