Long-term nitrogen addition causes the evolution of less-cooperative mutualists

Evolution

Volumn 69, Issue 3, 2015, Pages 631-642

  Weese, Dylan J ^a,b   Heath, Katy D ^c   Dentinger, Bryn T M ^d   Lau, Jennifer A ^b  

^a ST AMBROSE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d JODRELL LABORATORY   (United Kingdom)

Author keywords

Adaptation; Coevolution; Nitrogen deposition; Resource mutualism; Symbiosis

Indexed keywords

CHLOROPHYLL; COEVOLUTION; EXPERIMENTAL DESIGN; HUMAN ACTIVITY; LEGUME; LONG-TERM CHANGE; MUTUALISM; NATURE-SOCIETY RELATIONS; NITROGEN CYCLE; RHIZOBACTERIUM; TERRESTRIAL ECOSYSTEM;

RHIZOBIUM;

CHLOROPHYLL; FERTILIZER; NITROGEN;

BIOMASS; CHEMISTRY; CLOVER; ECOSYSTEM; EVOLUTION; FABACEAE; GENETICS; MICROBIOLOGY; NITROGEN CYCLE; PHYLOGENY; PHYSIOLOGY; RHIZOBIUM; SYMBIOSIS;

BIOLOGICAL EVOLUTION; BIOMASS; CHLOROPHYLL; ECOSYSTEM; FABACEAE; FERTILIZERS; NITROGEN; NITROGEN CYCLE; PHYLOGENY; RHIZOBIUM; SYMBIOSIS; TRIFOLIUM;

EID: 84924963186     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12594     Document Type: Article

References (58)

1. Akçay, E., and E. L. Simms . 2011. Negotiation, sanctions and context dependency in the legume-rhizobium mutualism. Am. Nat. 178:1-14.
2. Bullock, D. G., and D. S. Anderson . 1998. Evaluation of the Minolta SPAD-502 chloropyll meter for nitrogen management in corn. J. Plant Nutrit. 21:741-755.
3. Clark, C. M., and D. Tilman . 2008. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712-715.
4. Cleveland, C. C., A. R. Townsend, D. S. Schimel, H. Fisher, R. W. Howarth, L. O. Hedin, S. S. Perakis, E. F. Latty, J. C. Von Fischer, A. Elseroad, et al. 1999. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global. Biogeochem. Cycles 13:623-645.
5. Cusack, D. F., W. L. Silver, M. S Torn, S. D. Burton, and M. K. Fireston . 2011. Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621-632.
6. Denison, R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156:567-576.
7. Denison, R. F., and E. T. Kiers . 2004. Lifestyle alternative for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol. Lett. 237:187-193.
8. Diaz, R. J., and R. Rosenberg . 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926-929.
9. Dickson, T. L., and K. L. Gross . 2013. Plant community responses to long-term fertilization: changes in functional group abundance drive changes in species richness. Oecologia 173:1513-1520.
10. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
11. Elena, S. F., and R. E. Lenski . 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457-469.
12. Erisman, J. W., A. Bleeker, J. Gallowary, and M. S. Sutton . 2007. Reduced nitrogen in ecology and the environment. Env. Pollut. 150:140-149.
13. Frederickson, M. E. 2013. Rethinking mutualism stability: cheaters and the evolution of sanctions. Q. Rev. Biol. 88:269-295.
14. Galloway, J. N., F. J. Dentener, D. G. Capone, E. W. Boyer, R. W. Howarth, S. P. Seitzinger, G. P. Asner, C. C. Cleveland, P. A. Green, E. A. Holland, et al. 2004. Nitrogen cycles: past, present, and future. Biogeochemistry 70:153-226.
15. Galloway, J. N., A. R. Townsend, J. W. Erisman, M. Bekunda, Z. Cai, J. R. Freney, L. A. Martinelli, S. P. Seitzinger, and M. A. Sutton . 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889-892.
16. Galtier, N., M. Gouy, and C. Gautier . 1996. SeaView and Phylo_Win: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:53-548.
17. 2 partial pressure. New Phyt. 167:531-542.
18. Gouy, M., S. Guindon, and O. Gascuel . 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27:221-224.
19. Grman, E., J. A. Lau, D. R. Schoolmaster, and K. L. Gross . 2010. Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecol. Lett. 13:1400-1410.
20. Guindon, S., and O. Gascuel . 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
21. Halvorson, J. J., R. A. Black, J. L. Smith, and E. H. Franz . 1991. Nitrogenase activity, growth and carbon and nitrogen allocation in wintergreen and deciduous Lupin seedlings. Funct. Ecol. 5:554-651.
22. Heath, K. D., P. V. Burke, and J. R. Stinchcombe . 2012. Coevolutionary genetic variation in the legume-rhizobium transcriptome. Mol. Ecol. 21:4735-4747.
23. Heath, K. D., and J. R. Stinchcombe . 2014. Explaining mutualism variation: a new evolutionary paradox? Evolution 68:309-317.
24. Heath, K. D., and P. Tiffin . 2007. Context dependence in the coevolution plant and rhizobial mutualists. Proc. R. Soc. B 274:1905-1912.
25. Heath, K. D., and P. Tiffin . 2009. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 63:652-662.
26. Johnson, N. C. 1993. Can fertilization of soil select less mutualistic mycorrhizae? Ecol. Appl. 3:749-757.
27. Johnson, N. C., G. W. T. Wilson, M. A. Bowker, J. A. Wilson, and R. M. Miller . 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc. Natl. Acad. Sci. USA 107:2093-2098.
28. Kiers, E. T., S. A. West, and R. F. Denison . 2002. Mediating mutualisms: farm management practices and evolutionary changes in symbiont co-operation. J. Appl. Ecol. 39:745-754.
29. Kiers, E. T., R. A. Rousseau, S. A. West, and R. F. Denison . 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.
30. Kiers, E. T., M. G. Hutton, and R. F. Denison . 2007. Human selection and the relaxation of legume defences against ineffective rhizobia. Proc. Roy Soc. B 274:3119-3126.
31. Kiers, E.T., T. M. Palmer, A. R. Ives, J. F. Bruno, and J. L. Bronstein . 2010. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13:1459-1474.
32. Kjøller, R., L. O. Nilsson, K. Hansen, I. K. Schmidt, L. Vesterdal, and P. Gundersen . 2012. Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytol. 194:278-286.
33. Moulin, L., G. Bena, C. Boivin-Masson, and T. Stepkowski . 2004. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phylogenet. Evol. 30:720-732.
34. Neuhauser, C., and J. E. Fargione . 2004. A mutualism-parasitism continuum model and its application to plant-mycorrhizae interactions. Ecol. Model. 177:337-352.
35. Oono, R., Dnison, R. F., & Kiers, E. T. 2009. Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytologist. 183:967-979.
36. 2) by nonreproductive symbiotic rhizobia triggers sanctions that reduce fitness of their reproductive clonemates. Proc. Roy Soc. B 278:2698-2703.
37. Rabalais, N. N. 2002. Nitrogen in aquatic ecosystems. Ambio 31:102-112.
38. Ratcliff, W. C., K. Underbakke, and R. F. Denison . 2011. Measuring the fitness of symbiotic rhizobia. Symbiosis 55:85-90.
39. Sachs, J. L., and E. L. Simms . 2006. Pathways to mutualism breakdown. Trends Ecol. Evol. 21:585-592.
40. Sachs, J. L., U. G. Mueller, T. P. Wilcox, and J. J. Bull . 2004. The evolution of cooperation. Quart. Rev. Biol. 79: 135-160.
41. Sachs, J. L., S. W. Kembel, A. H. Lau, and E. L. Simms . 2009. In situ phylogenetic structure and diversity of wild bradyrhizobium communities. Appl. Environ. Microbiol. 75:4727-4735.
42. Sachs, J. L., M. O. Ehinger, and E. L. Simms . 2010. Origins of cheating and loss of symbiosis in wild Bradyrhizobium. J. Evol. Biol. 23:1075-1089.
43. Sachs, J. L., J. E. Russell, and A. C. Hollowell . 2011. Evolutionary instability of symbiotic function in Bradyrhizobium japonicum. PLoS One 6:e26370.
44. Schlesinger, W. H. 2009. On the fate of anthropogenic nitrogen. Proc. Natl. Acad. Sci. USA 106:203-208.
45. Shimodaira, H., and M. Hasegawa . 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114-1116.
46. Simms, E. L., D. L. Taylor, J. Povich, R. P. Shefferson, J. L. Sachs, Y. Tausczik, and M. Urbina . 2006. An empirical test of partner choice mechanisms in a legume-rhizobium interaction. Proc. Roy. Soc. B. 273:77-81.
47. Six, D. L. 2009. Climate change and mutualism. Nat. Rev. Microbio. 7:686.
48. Sterner, R. W., and J. J. Elser . 2002. Ecological stoichiometry: the biology of the elements from molecules to the biosphere. Princeton Univ. Press, Princeton, NJ.
49. Strauss, S. Y., J. A. Lau, T. W. Schoener, and P. Tiffin . 2008. Evolution in ecological field experiments: implications for effect size. Ecol. Lett. 11:199-207.
50. Streeter, J. 1988. Inhibition of legume nodule formation and N-2 fixation by nitrate. Crit. Rev. Plant. Sci. 7:1-23.
51. Swiader, J. M., and A. Moore . 2002. SPAD-chlorophyll response to nitrogen fertilization and evaluation of nitrogen status in dryland and irrigated pumpkins. J. Plant Nutrit. 25:1089-1100.
52. Swofford, D. L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0 b10. Sinauer Associates, Sunderland, MA.
53. Thrall, P. H., D. A. Millsom, A. C. Jeavons, M. Waayers, G. R. Harvey, D. J. Bagnall, and J. Brockwell . 2005. Seed inoculation with effective root-nodule bacteria enhances revegetation success. J. Appl. Ecol. 42:740-751.
54. Thrall, P. H., M. E. Hochberg, J. J. Burdon, and J. D. Bever . 2007. Coevolution of symbiotic mutualists and parasites in a community context. TREE 22:120-126.
55. Vitousek, P. M., J. D. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger, and D. G. Tilman . 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol. App. 7:737-750.
56. Wernegreen, J. J., and M. A. Riley . 1999. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for genetic coherence of rhizobial lineages. Mol. Biol. Evol. 16:98-113.
57. West, S. A., E. T. Kiers, E. L. Simms, and R. F. Denison . 2002. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc. R. Soc. Lond. B 269:685-694.
58. Zechmeister-Boltenstern, S., K. Michel, and M. Pfeffer . 2011. Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen deposition. Plant Soil 343:37-50.