Differentiating genetic and environmental drivers of plant-pathogen community interactions

Journal of Ecology

Volumn 102, Issue 5, 2014, Pages 1300-1309

  Busby, Posy E ^a   Newcombe, George ^b   Dirzo, Rodolfo ^a   Whitham, Thomas G ^c  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

Determinants of plant community diversity and structure; Disease; Foundation species; Genotype environment interactions; Local adaptation; Pathogen communities; Populus; Scaling

Indexed keywords

COMMUNITY COMPOSITION; DECIDUOUS TREE; DISEASE RESISTANCE; ENVIRONMENTAL EFFECT; ENVIRONMENTAL FACTOR; FUNGUS; GARDEN; GENETIC STRUCTURE; GENOTYPE; GENOTYPE-ENVIRONMENT INTERACTION; GREENHOUSE ECOSYSTEM; HOST-PATHOGEN INTERACTION; LOCAL ADAPTATION; PATHOGEN;

ARTHROPODA; POPULUS; POPULUS ANGUSTIFOLIA;

EID: 84906043912     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12270     Document Type: Article

References (67)

1. Adams, R.I., Goldberry, S., Whitham, T.G., Zinkgraf, M.S. & Dirzo, R. (2011) Hybridization among dominant tree species correlates positively with understory plant diversity. American Journal of Botany, 98, 1623-1632.
2. Agrawal, A. (2003) Community genetics: new insights into community ecology by integrating population genetics. Ecology, 84, 543-544.
3. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
4. Anderson, M.J. (2005) PERMANOVA: A FORTRAN Computer Program for Permutational Multivariate Analysis of Variance. Department of Statistics, University of Auckland, Auckland, New Zealand.
5. Antonovics, J. (1992) Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics (eds R.S. Fritz & E.L. Simms). University of Chicago Press, Chicago, IL, USA.
6. Bangert, R., Allan, G., Turek, R., Wimp, G., Meneses, N., Martinsen, G., Keim, P. & Whitham, T.G. (2006) From genes to geography: a genetic similarity rule for arthropod community structure at multiple geographic scales. Molecular Ecology, 15, 4215-4228.
7. Barbour, R.C., Storer, M.J. & Potts, B.M. (2009a) Relative importance of tree genetics and microhabitat on macrofungal biodiversity on coarse woody debris. Oecologia, 160, 335-342.
8. Barbour, R., O'Reilly-Wapstra, J., Little, D., Jordan, G., Steane, D., Humphreys, J., Bailey, J., Whitham, T.G. & Potts, B. (2009b) A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology, 90, 1762-1772.
9. Bell, G. (1992) Five Properties of Environments (eds P. Grant & H. Horn). Princeton University Press, Princeton, New Jersey, USA.
10. Bernhardsson, C., Robinson, K.M., Abreu, I.N., Jansson, S., Albrectsen, B.R. & Ingvarsson, P.K. (2013) Geographic structure in metabolome and herbivore community co-occurs with genetic structure in plant defence genes. Ecology Letters, 16, 791-798.
11. Burdon, J. & Chilvers, G. (1982) Host density as a factor in plant disease ecology. Annual Review of Phytopathology, 20, 143-166.
12. Burdon, J. & Thrall, P. (1999) Spatial and temporal patterns in coevolving plant and pathogen associations. The American Naturalist, 153, S15-S33.
13. Busby, P.E., Aime, M.C. & Newcombe, G. (2012) Foliar pathogens of Populus angustifolia are consistent with a hypothesis of Beringian migration into North America. Fungal Biology, 116, 792-801.
14. Busby, P.E., Newcombe, G., Dirzo, R. & Whitham, T.G. (2013a) Genetic basis of pathogen community structure for foundation tree species in a common garden and in the wild. Journal of Ecology, 101, 867-877.
15. Busby, P.E., Zimmerman, N., Weston, D.J., Jawdy, S.S., Houbraken, J. & Newcombe, G. (2013b) Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen, Drepanopeziza populi. Ecosphere, 4, 125.
16. Busby, P.E., Lamit, L.J., Keith, A.R., Newcombe, G., Gehring, C.A., Whitham, T.G. & Dirzo, R. (in press) Genetics-based interactions among plants, pathogens and herbivores define arthropod community structure. Ecology.
17. Clarke, K. (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 117-143.
18. Clausen, J., Keck, D. & Hiesey, W. (1948) Experimental Studies on the Nature of Species. III. Environmental Responses of Climatic Races of Achillea. Carnegie Inst, Washington D.C.
19. Conner, J.K. & Hartl, D.L. (2004) A Primer of Ecological Genetics. Sinauer Associates Inc, Sunderland, MA, USA.
20. Craig, T., Itami, J. & Horner, J. (2007) Geographic variation in the evolution and coevolution of a tritrophic interaction. Evolution, 61, 1137-1152.
21. Dayton, P. (1972) Toward an understanding of community resilience and the potential effects to the benthos at McMurdo Sound, Antarctica. Proceedings of the Colloquium on Conservation Problems in Antarctica (ed. B.C. Parker). Allen Press, Lawrence, KS.
22. Dirzo, R. & Domínguez, C. (1995) Plant-Herbivore Interactions in Mesoamerican Tropical Dry Forests (eds S. Bullock, H. Mooney & E. Medina). Cambridge University Press, Cambridge, UK.
23. Ellison, A., Bank, M., Clinton, B., Colburn, E., Elliott, K., Ford, C. et al. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment, 3, 479-486.
24. Evans, L.M., Allan, G.J., Meneses, N., Max, T.L. & Whitham, T.G. (2013) Herbivore host-associated genetic differentiation depends on the scale of plant genetic variation examined. Evolutionary Ecology, 27, 65-81.
25. Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L. & Gurr, S.J. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186-194.
26. Fritz, R. (1988) Genetic variation among plants and insect community structure: willows and sawflies. Ecology, 69, 845-856.
27. Gehring, C., Mueller, R. & Whitham, T.G. (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia, 149, 158-164.
28. Geiger, H. & Heun, M. (1989) Genetics of quantitative resistance to fungal diseases. Annual Review of Phytopathology, 27, 317-341.
29. Grady, K.C., Ferrier, S.M., Kolb, T.E., Hart, S.C., Allan, G.J. & Whitham, T.G. (2011) Genetic variation in productivity of foundation riparian species at the edge of their distribution: implications for restoration and assisted migration in a warming climate. Global Change Biology, 17, 3724-3735.
30. Hamilton, M.G., Williams, D.R., Tilyard, P.A., Pinkard, E.A., Wardlaw, T.J., Glen, M., Vaillancourt, R.E. & Potts, B.M. (2013) A latitudinal cline in disease resistance of a host tree. Heredity, 110, 372-379.
31. Harvell, C., Mitchell, C., Ward, J., Altizer, S., Dobson, A., Ostfeld, R. & Samuel, M. (2002) Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.
32. Hereford, J. (2009) A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579-588.
33. Hoeksema, J.D. & Forde, S.E. (2008) A meta-analysis of factors affecting local adaptation between interacting species. The American Naturalist, 171, 275-290.
34. Hughes, A.R., Inouye, B.D., Johnson, M.T.J., Underwood, N. & Vellend, M. (2008) Ecological consequences of genetic diversity. Ecology Letters, 11, 609-623.
35. Johnson, M. & Agrawal, A. (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology, 86, 874-885.
36. Johnson, M., Lajeunesse, M. & Agrawal, A. (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecology Letters, 9, 24-34.
37. Kaltz, O. & Shykoff, J.A. (1998) Local adaptation in host-parasite systems. Heredity, 81, 361-370.
38. Kawecki, T.J. & Ebert, D. (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225-1241.
39. Keith, A., Bailey, J. & Whitham, T.G. (2010) A genetic basis to community repeatability and stability. Ecology, 91, 3398-3406.
40. Laine, A. (2005) Spatial scale of local adaptation in a plant-pathogen metapopulation. Journal of Evolutionary Biology, 18, 930-938.
41. Lovett, G.M., Canham, C.D., Arthur, M.A., Weathers, K.C. & Fitzhugh, R.D. (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience, 56, 395-405.
42. Maddox, G. & Root, R. (1987) Resistance to 16 diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia, 72, 8-14.
43. Menge, B.A. & Olson, A.M. (1990) Role of scale and environmental factors in regulation of community structure. Trends in Ecology and Evolution, 5, 52-57.
44. Newcombe, G. & Bradshaw, H. Jr (1996) Quantitative trait loci conferring resistance in hybrid poplar to Septoria populicola, the cause of leaf spot. Canadian Journal of Forest Research, 26, 1943-1950.
45. Nuismer, S.L., Thompson, J.N. & Gomulkiewicz, R. (2000) Coevolutionary clines across selection mosaics. Evolution, 54, 1102-1115.
46. O'Neill, G.A., Hamann, A. & Wang, T. (2008) Accounting for population variation improves estimates of the impact of climate change on species' growth and distribution. Journal of Applied Ecology, 45, 1040-1049.
47. Ostry, M. (1987) Biology of Septoria musiva and Marssonina brunnea in hybrid Populus plantations and control of Septoria canker in nurseries. European Journal of Forest Pathology, 17, 158-165.
48. Ostry, M. & McNabb, H. Jr (1986) Populus species and hybrid clones resistant to Melampsora, Marssonina, and Septoria. USDA Forest Service research paper NC-United States, North Central Forest Experiment Station (USA).
49. Parker, M. (1985) Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution, 39, 713-723.
50. Quaedvlieg, W., Verkley, G.J.M., Shin, H.-D., Barreto, R.W., Alfenas, A.C., Swart, W.J., Groenewald, J.Z. & Crous, P.W. (2013) Sizing up Septoria. Studies in Mycology, 75, 307-390.
51. Rasband, W.S. (1997-2014) ImageJ. U.S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/.
52. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
53. Schweitzer, J., Bailey, J., Fischer, D., LeRoy, C., Lonsdorf, E., Whitham, T.G. & Hart, S. (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology, 89, 773-781.
54. Smith, D.S., Bailey, J.K., Shuster, S.M. & Whitham, T.G. (2011) A geographic mosaic of trophic interactions and selection: trees, aphids and birds. Journal of Evolutionary Biology, 24, 422-429.
55. Sork, V.L., Stowe, K.A. & Hochwender, C. (1993) Evidence for local adaptation in closely adjacent subpopulations of northern red oak (Quercus rubra L.) expressed as resistance to leaf herbivores. The American Naturalist, 142, 928-936.
56. Soubeyrand, S., Laine, A.L., Hanski, I. & Penttinen, A. (2009) Spatiotemporal structure of host-pathogen interactions in a metapopulation. The American Naturalist, 174, 308-320.
57. Tack, A.J.M., Gripenberg, S. & Roslin, T. (2012a) Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecology Letters, 15, 177-185.
58. Tack, A.J.M., Johnson, M.T. & Roslin, T. (2012b) Sizing up community genetics: it's a matter of scale. Oikos, 121, 481-488.
59. Tack, A., Ovaskainen, O., Pulkkinen, P. & Roslin, T. (2010) Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology, 91, 2660-2672.
60. Tack, A.J.M., Thrall, P.H., Barrett, L.G., Burdon, J.J. & Laine, A.L. (2012c) Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. Journal of Evolutionary Biology, 25, 1918-1936.
61. Thompson, J.N. (1997) Evaluating the dynamics of coevolution among geographically structured populations. Ecology, 78, 1619-1623.
62. Thompson, J.N. (2005) The Geographic Mosaic of Coevolution (Interspecific Interactions), 1st edn. University Of Chicago Press, Chicago, Illinois.
63. Whitham, T.G., Young, W., Martinsen, G., Gehring, C., Schweitzer, J., Shuster, S., Wimp, G., Fischer, D., Bailey, J., Lindroth, R., Woolbright, S. & Kuske, C. (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology, 84, 559-573.
64. Whitham, T.G., Bailey, J.K., Schweitzer, J.A., Shuster, S.M., Bangert, R.K., Leroy, C.J. et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics, 7, 510-523.
65. Whitham, T.G., Gehring, C.A., Lamit, L.J., Wojtowicz, T., Evans, L.M., Keith, A.R. & Smith, D.S. (2012) Community specificity: life and afterlife effects of genes. Trends in Plant Science, 17, 271-281.
66. Zar, J. (1996) Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.
67. Zytynska, S.E., Fay, M.F., Penney, D. & Preziosi, R.F. (2011) Genetic variation in a tropical tree species influences the associated epiphytic plant and invertebrate communities in a complex forest ecosystem. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 366, 1329-1336.