Evolutionary Ecology

, Volume 26, Issue 3, pp 529–544 | Cite as

Local adaptation across a fertility gradient is influenced by soil biota in the invasive grass, Bromus inermis

  • Mark E. Sherrard
  • Hafiz Maherali
Original Paper


Biotic soil factors, such as fungi, bacteria and herbivores affect resource acquisition and fitness in plants, yet little is known of their role as agents of selection. Evolutionary responses to these selective agents could be an important mechanism that explains the success of invasive species. In this study, we tested whether populations of the invasive grass Bromus inermis are adapted to their home soil environment, and whether biotic factors influence the magnitude of this adaptation. We selected three populations growing at sites that differed in soil fertility and grew individuals from each population in each soil. To assess whether biotic factors influence the magnitude of adaptation, we also grew the same populations in sterilized field soil. To further examine the role of one element of the soil biota (fungi) in local adaptation, we measured colonization by arbuscular mycorrhizal (AM) and septate fungi, and tested whether the extent of colonization differed between local and foreign plants. In non-sterilized (living) soil, there was evidence of a home site advantage because local plants produced significantly more biomass than at least one of the two populations of foreign plants in all three soil origins. By contrast, there was no evidence of a home site advantage in sterilized soil because local plants never produced significantly more biomass than either population of foreign plants. Fungal colonization differed between local and foreign plants in the living soil and this variation corresponded with biomass differences. When local plants produced more biomass than foreign plants, they were also less intensively colonized by AM fungi. Colonization by septate fungi did not vary between local and foreign plants. Our results suggest that biotic soil factors are important causes of plant adaptation, and that selection for reduced interactions with mycorrhizae could be one mechanism through which adaptation to a novel environment occurs.


Arbuscular mycorrhizal fungi Common garden Invasion Local adaptation Nutrient availability Plant–soil interactions Septate fungi 



We thank C. M. Caruso, J. A. Newman and J. N. Klironomos for helpful discussions and comments on earlier versions of this manuscript. We thank M. Arcand, A. Clark, R. Germain, A. Lambert, L. MacDonald and M. Mucci for assistance in the greenhouse, field and lab. This work was supported by the Natural Science and Engineering Research Council of Canada and grants from the Canadian Foundation for Innovation and the Ontario Innovation Trust.

Supplementary material

10682_2011_9518_MOESM1_ESM.doc (162 kb)
Supplementary material 1 (DOC 162 kb)


  1. Antonovics J, Bradshaw AE (1970) Evolution in closely adjacent plant populations. VIII. Clinal patterns at a mine boundary. Heredity 25:349–362CrossRefGoogle Scholar
  2. Bennington CC, McGraw JB (1995) Natural selection and ecotypic differentiation in Impatiens pallida. Ecol Monogr 65:303–324CrossRefGoogle Scholar
  3. Berns AE, Philipp H, Narres H-D et al (2008) Effect of gamma-sterilization and autoclaving on soil organic matter structure as studied by solid state NMR, UV and fluorescence spectroscopy. Eur J Soil Sci 59:540–550CrossRefGoogle Scholar
  4. Bildusas IJ, Dixon RK, Pfleger FL et al (1986) Growth, nutrition and gas exchange of Bromus inermis inoculated with Glomus fasciculatum. New Phytol 102:303–311CrossRefGoogle Scholar
  5. Brundrett M (1994) Clearing and staining mycorrhizal roots. In: Brundrett M, Melville L, Peterson L (eds) Practical methods in mycorrhizal research. Mycologue Publications, Waterloo, pp 42–46Google Scholar
  6. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  7. Buswell JM, Moles At, Hartlet S (2011) Is rapid evolution common in introduced plant species? J Ecol 99:214–224CrossRefGoogle Scholar
  8. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  9. Clausen J, Keck DD, Heisey WM (1948) Experimental studies on the nature of species. III. Environmental responses of climactic races of Achillea. Carnegie Institute of Washington Publication 581:129Google Scholar
  10. Donovan LA, Ludwig F, Rosenthal DM et al (2009) Phenotypic selection on leaf ecophysiological traits in Helianthus. New Phytol 183:868–879PubMedCrossRefGoogle Scholar
  11. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  12. Felsenstein J (1976) The theoretical population genetics of variable selection and migration. Annu Rev Genet 10:253–280PubMedCrossRefGoogle Scholar
  13. Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621CrossRefGoogle Scholar
  14. Gist GR, Smith RM (1948) Root development of several common forage grasses to a depth of eighteen inches. J Am Soc Agron 40:1036–1042CrossRefGoogle Scholar
  15. Grime PJ (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  16. Grime PJ (2001) Plant strategies, vegetation processes and ecosystem properties, 2nd edn. Wiley, ChichesterGoogle Scholar
  17. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588PubMedCrossRefGoogle Scholar
  18. Johnson N (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757CrossRefGoogle Scholar
  19. Johnson NC, Wilson GWT, Bowker MA et al (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci USA 107:2093–2098PubMedCrossRefGoogle Scholar
  20. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Let 7:1225–1241CrossRefGoogle Scholar
  21. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  22. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  23. Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. In: Begon M, Fitter AH (eds) Advances in Ecological Research Volume 23. Academic Press Ltd., London, pp 187–261CrossRefGoogle Scholar
  24. Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3:e4010PubMedCrossRefGoogle Scholar
  25. Lenssen JPM, van Kleunen M, Fischer M et al (2004) Local adaptation of the clonal plant Ranunculus reptans to flooding along a small-scale gradient. J Ecol 92:696–706CrossRefGoogle Scholar
  26. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277CrossRefGoogle Scholar
  27. Macel M, Lawson CS, Mortimer SR et al (2007) Climate vs. soil factors in local adaptation of two common plant species. Ecology 88:424–433PubMedCrossRefGoogle Scholar
  28. Maron JL (1998) Individual and joint effects of below- and above-ground insect herbivory on perennial plant fitness. Ecology 79:1281–1293CrossRefGoogle Scholar
  29. Maron JL, Vilà M, Bommarco R et al (2004) Rapid evolution of an invasive plant. Ecol Mono 74:261–280CrossRefGoogle Scholar
  30. McGonigle TP, Miller MH, Evans DG et al (1990) A method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  31. McGraw JB, Chapin FS III (1989) Competitive ability and adaptation to fertile and infertile soils in two Eriophorum species. Ecology 70:736–749CrossRefGoogle Scholar
  32. McKone MJ (1985) Reproductive biology of several bromegrasses (Bromus): breeding system, pattern of fruit maturation, and seed set. Am J Bot 72:1334–1339CrossRefGoogle Scholar
  33. McNamara NP, Black HIJ, Beresford NA et al (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24:117–132CrossRefGoogle Scholar
  34. Newell LC, Keim FD (1943) Field performance of bromegrass strains from different regional seed sources. J Am Soc Agron 35:420–434CrossRefGoogle Scholar
  35. Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793PubMedCrossRefGoogle Scholar
  36. Newsham KK, Fitter AH, Watkinson AR (1994) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000Google Scholar
  37. Otfinowski R, Kenkel NC, Catling PM (2007) The biology of Canadian weeds. 134. Bromus inermis Leyss. Can J Plant Sci 87:183–198CrossRefGoogle Scholar
  38. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  39. Pregitzer CC, Bailey JK, Hart SC et al (2010) Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evol Ecol 24:1045–1059CrossRefGoogle Scholar
  40. Pringle A, Bever JD, Gardes M et al (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Syst 40:699–715CrossRefGoogle Scholar
  41. Rausher MD, Simms EL (1989) The evolution of resistance to herbivory in Ipomoea purpurea I. attempts to detect selection. Evolution 43:563–572CrossRefGoogle Scholar
  42. Reinhart KO, Royo AA, van der Putten WH et al (2005) Soil feedback and pathogen activity in Prunus serotina throughout its native range. J Ecol 93:890–898CrossRefGoogle Scholar
  43. Salonius PO, Robin JB, Chase FE (1967) A comparison of autoclaved and gamma-irradiated soils as media for microbial colonization experiments. Plant Soil 27:239–248CrossRefGoogle Scholar
  44. Schemske DW (1984) Population structure and local selection in Impatiens pallida (Balsaminaceae), a selfing annual. Evolution 38:817–832CrossRefGoogle Scholar
  45. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New YorkGoogle Scholar
  46. Schultz PA, Miller RM, Jastrow JD et al (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am J Bot 88:1650–1656PubMedCrossRefGoogle Scholar
  47. Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062PubMedCrossRefGoogle Scholar
  48. Sherrard ME (2010) Physiological adaptation to biotic and abiotic soil factors in Bromus inermis. Dissertation, University of Guelph, Guelph, CanadaGoogle Scholar
  49. Snaydon RW, Bradshaw AD (1962) Differences between natural populations of Trifolium repens L. in response to mineral nutrients. J Exp Bot 13:422–434CrossRefGoogle Scholar
  50. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  51. Troelstra SR, Wagenaar R, Smant W et al (2001) Interpretation of bioassays in the study of interactions between soil organisms and plants: involvement of nutrient factors. New Phytol 150:697–706CrossRefGoogle Scholar
  52. Turkington R, Harper JL (1979) The growth, distribution and neighbour relationships of Trifolium repens in a permanent pasture. IV. Fine-scale biotic differentiation. J Ecol 67:245–254CrossRefGoogle Scholar
  53. Wade MJ, Kalisz S (1990) The causes of natural selection. Evolution 44:1947–1955CrossRefGoogle Scholar
  54. Wolfe BE, Husband BC, Klironomos JN (2005) Effects of a belowground mutualism on an aboveground mutualism. Ecol Let 8:218–223CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  2. 2.Department of BiologyUniversity of Northern IowaCedar FallsUSA

Personalised recommendations