, Volume 170, Issue 3, pp 835–845 | Cite as

Phylogenetic niche conservatism in C4 grasses

  • Hui Liu
  • Erika J. Edwards
  • Robert P. Freckleton
  • Colin P. Osborne
Global change ecology - Original research


Photosynthetic pathway is used widely to discriminate plant functional types in studies of global change. However, independent evolutionary lineages of C4 grasses with different variants of C4 photosynthesis show different biogeographical relationships with mean annual precipitation, suggesting phylogenetic niche conservatism (PNC). To investigate how phylogeny and photosynthetic type differentiate C4 grasses, we compiled a dataset of morphological and habitat information of 185 genera belonging to two monophyletic subfamilies, Chloridoideae and Panicoideae, which together account for 90 % of the world’s C4 grass species. We evaluated evolutionary variance and covariance of morphological and habitat traits. Strong phylogenetic signals were found in both morphological and habitat traits, arising mainly from the divergence of the two subfamilies. Genera in Chloridoideae had significantly smaller culm heights, leaf widths, 1,000-seed weights and stomata; they also appeared more in dry, open or saline habitats than those of Panicoideae. Controlling for phylogenetic structure showed significant covariation among morphological traits, supporting the hypothesis of phylogenetically independent scaling effects. However, associations between morphological and habitat traits showed limited phylogenetic covariance. Subfamily was a better explanation than photosynthetic type for the variance in most morphological traits. Morphology, habitat water availability, shading, and productivity are therefore all involved in the PNC of C4 grass lineages. This study emphasized the importance of phylogenetic history in the ecology and biogeography of C4 grasses, suggesting that divergent lineages need to be considered to fully understand the impacts of global change on plant distributions.


Phylogenetic niche conservatism C3/C4 photosynthesis Poaceae Morphology Habitat 



We gratefully thank Samuel Taylor for discussion on statistics. This work was funded by a UK/China Excellence Scholarship from the China Scholarship Council and the UK Government Department for Innovation, Universities and Skills (now Department for Business, Innovation and Skills).

Supplementary material

442_2012_2337_MOESM1_ESM.pdf (595 kb)
Supplementary material 1 (PDF 570 kb)


  1. 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 162:543–557. doi: 10.1111/j.1095-8339.2010.01041.x CrossRefGoogle Scholar
  2. Burns J, Ashman T-L, Steets J, Harmon-Threatt A, Knight T (2011) A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions. Oecologia. doi: 10.1007/s00442-011-1929-9 PubMedGoogle Scholar
  3. Cabido M, Pons E, Cantero JJ, Lewis JP, Anton A (2008) Photosynthetic pathway variation among C4 grasses along a precipitation gradient in Argentina. J Biogeogr 35:131–140. doi: 10.1111/j.1365-2699.2007.01760.x Google Scholar
  4. Cavender-Bares J, Keen A, Miles B (2006) Phylogenetic structure of Floridian plant communities depends on taxonomic and spatial scale. Ecology 87:109–122. doi: 10.1890/0012-9658(2006)87[109:PSOFPC]2.0.CO;2 CrossRefGoogle Scholar
  5. Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43. doi: 10.1016/j.cub.2007.11.058 PubMedCrossRefGoogle Scholar
  6. Christin PA, Salamin N, Kellogg EA, Vicentini A, Besnard G (2009) Integrating phylogeny into studies of C4 variation in the grasses. Plant Physiol 149:82–87. doi: 10.1104/pp.108.128553 PubMedCrossRefGoogle Scholar
  7. Christin PA, Freckleton RP, Osborne CP (2010) Can phylogenetics identify C4 origins and reversals? Trends Ecol Evol 25:403–409. doi: 10.1016/j.tree.2010.04.007 PubMedCrossRefGoogle Scholar
  8. Clayton WD, Harman KT, Williamson H (2006 onwards) GrassBase—the online world grass flora.
  9. Cooper N, Jetz W, Freckleton RP (2010) Phylogenetic comparative approaches for studying niche conservatism. J Evol Biol 23:2529–2539. doi: 10.1111/j.1420-9101.2010.02144.x PubMedCrossRefGoogle Scholar
  10. Cooper N, Freckleton RP, Jetz W (2011) Phylogenetic conservatism of environmental niches in mammals. Proc R Soc Lond B. doi: 10.1098/rspb.2010.2207 Google Scholar
  11. Crisp MD, Arroyo MTK, Cook LG, Gandolfo MA, Jordan GJ, McGlone MS, Weston PH, Westoby M, Wilf P, Linder HP (2009) Phylogenetic biome conservatism on a global scale. Nature 458:754–756. doi: 10.1038/nature07764 PubMedCrossRefGoogle Scholar
  12. Cross RA (1980) Distribution of subfamilies of Gramineae in the Old World. Kew Bull 35:279–289. Google Scholar
  13. Donoghue MJ (2008) A phylogenetic perspective on the distribution of plant diversity. Proc Natl Acad Sci USA 105:11549–11555. doi: 10.1073/pnas.0801962105 PubMedCrossRefGoogle Scholar
  14. Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc Natl Acad Sci USA 107:2532–2537. doi: 10.1073/pnas.0909672107 PubMedCrossRefGoogle Scholar
  15. Edwards EJ, Still CJ, Donoghue MJ (2007) The relevance of phylogeny to studies of global change. Trends Ecol Evol 22:243–249. doi: 10.1016/j.tree.2007.02.002 PubMedCrossRefGoogle Scholar
  16. Edwards EJ, Osborne CP, Stromberg CAE, Smith SA, Consortium CG (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591. doi: 10.1126/science.1177216 PubMedCrossRefGoogle Scholar
  17. Ehleringer JR (1978) Implications of quantum yield differences on distributions of C3 and C4 grasses. Oecologia 31:255–267. doi: 10.1007/BF00346246 CrossRefGoogle Scholar
  18. Ellis RP, Vogel JC, Fuls A (1980) Photosynthetic pathways and the geographical distribution of grasses in South West Africa/Namibia. S Afr J Sci 76:307–314Google Scholar
  19. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726. doi: 10.1086/343873 PubMedCrossRefGoogle Scholar
  20. Gibbs Russell GE (1988) Distribution of subfamilies and tribes of Poaceae in southern Africa. Monogr Syst Bot 25:555–566Google Scholar
  21. Giussani LM, Cota-Sanchez JH, Zuloaga FO, Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012PubMedCrossRefGoogle Scholar
  22. Grass Phylogeny Working Group II (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. doi: 10.1111/j.1469-8137.2011.03972.x CrossRefGoogle Scholar
  23. Hartley W (1950) The global distribution of tribes of the Gramineae in relation to historical and environmental factors. Aust J Agric Res 1:355–373. doi: 10.1071/AR9500355 CrossRefGoogle Scholar
  24. Hartley W (1958a) Studies on the origin, evolution and distribution of the Gramineae. I The tribe Andropogoneae. Aust J Bot 6:116–128. doi: 10.1071/BT9580116 CrossRefGoogle Scholar
  25. Hartley W (1958b) Studies on the origin, evolution, and distribution of the Gramineae. II The tribe Paniceae. Aust J Bot 6:343–357. doi: 10.1071/BT9580343 CrossRefGoogle Scholar
  26. Hartley W, Slater C (1960) Studies on the origin, evolution, and distribution of the Gramineae. III The tribes of the subfamily Eragrostoideae. Aust J Bot 8:256–276. doi: 10.1071/BT9600256 CrossRefGoogle Scholar
  27. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  28. Hattersley PW (1983) The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57:113–128. doi: 10.1007/BF00379569 CrossRefGoogle Scholar
  29. Hill S, Kotanen P (2011) Phylogenetic structure predicts capitular damage to Asteraceae better than origin or phylogenetic distance to natives. Oecologia 166:843–851. doi: 10.1007/s00442-011-1927-y PubMedCrossRefGoogle Scholar
  30. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003. doi: 10.1111/j.1461-0248.2008.01229.x PubMedCrossRefGoogle Scholar
  31. Osborne CP, Freckleton RP (2009) Ecological selection pressures for C4 photosynthesis in the grasses. Proc R Soc Lond B 276:1753–1760. doi: 10.1098/rspb.2008.1762 CrossRefGoogle Scholar
  32. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. doi: 10.1038/44766 PubMedCrossRefGoogle Scholar
  33. Peterson PM, Romaschenko K, Johnson G (2010) A classification of the Chloridoideae (Poaceae) based on multi-gene phylogenetic trees. Mol Phylogenet Evol 55:580–598. doi: 10.1016/j.ympev.2010.01.018 PubMedCrossRefGoogle Scholar
  34. Poorter H, De Jong ROB (1999) A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity. New Phytol 143:163–176. doi: 10.1046/j.1469-8137.1999.00428.x CrossRefGoogle Scholar
  35. Price T (1997) Correlated evolution and independent contrasts. Philos Trans R Soc Lond Bi 352:519–529. doi: 10.1098/rstb.1997.0036 CrossRefGoogle Scholar
  36. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591–601. doi: 10.1080/10635150802302427 PubMedCrossRefGoogle Scholar
  37. Royal Botanic Gardens Kew (2009) Seed Information Database (SID). Version 7.1. Accessed May 2009
  38. Sage RF, Li M, Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic, San Diego, pp 551–584CrossRefGoogle Scholar
  39. Sankaran M, Ratnam J, Hanan N (2008) Woody cover in African savannas: the role of resources, fire and herbivory. Glob Ecol Biogeogr 17:236–245. doi: 10.1111/j.1466-8238.2007.00360.x CrossRefGoogle Scholar
  40. Silvertown J, McConway K, Gowing D, Dodd M, Fay MF, Joseph JA, Dolphin K (2006) Absence of phylogenetic signal in the niche structure of meadow plant communities. Proc R Soc Lond B 273:39–44. doi: 10.1098/rspb.2005.3288 CrossRefGoogle Scholar
  41. Sitch S, Huntingford C, Gedney N, Levy PE, Lomas M, Piao SL, Betts R, Ciais P, Cox P, Friedlingstein P, Jones CD, Prentice IC, Woodward FI (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five dynamic global vegetation models (DGVMs). Glob Change Biol 14:2015–2039. doi: 10.1111/j.1365-2486.2008.01626.x CrossRefGoogle Scholar
  42. Still CJ, Berry JA, Collatz GJ, DeFries RS (2003) Global distribution of C3 and C4 vegetation: carbon cycle implications. Glob Biogeochem Cy 17:1006–1014. doi: 10.1029/2001GB001807 CrossRefGoogle Scholar
  43. Taub DR (2000) Climate and the USA distribution of C4 grass subfamilies and decarboxylation variants of C4 photosynthesis. Am J Bot 87:1211–1215PubMedCrossRefGoogle Scholar
  44. Taylor SH, Hulme SP, Rees M, Ripley BS, Woodward FI, Osborne CP (2010) Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytol 185:780–791. doi: 10.1111/j.1469-8137.2009.03102.x PubMedCrossRefGoogle Scholar
  45. Taylor SH, Ripley BS, Woodward FI, Osborne CP (2011) Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment. Plant Cell Environ 34:65–75. doi: 10.1111/j.1365-3040.2010.02226.x PubMedCrossRefGoogle Scholar
  46. 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 14:2963–2977. doi: 10.1111/j.1365-2486.2008.01688.x CrossRefGoogle Scholar
  47. Watson L, Dallwitz MJ (1992 onwards) The grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. Version: 26th Nov 2008. Available online: Accessed 11th Nov 2006
  48. Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539. doi: 10.1146/annurev.ecolsys.36.102803.095431 CrossRefGoogle Scholar
  49. Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Davies TJ, Grytnes JA, Harrison SP, Hawkins BA, Holt RD, McCain CM, Stephens PR (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324. doi: 10.1111/j.1461-0248.2010.01515.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Hui Liu
    • 1
  • Erika J. Edwards
    • 2
  • Robert P. Freckleton
    • 1
  • Colin P. Osborne
    • 1
  1. 1.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  2. 2.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA

Personalised recommendations