Access the full text.
Sign up today, get DeepDyve free for 14 days.
Joel Sachs, M. Ehinger, E. Simms (2010)
Origins of cheating and loss of symbiosis in wild BradyrhizobiumJournal of Evolutionary Biology, 23
Robert Edgar (2004)
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Nucleic acids research, 32 5
R. Kjøller, L. Nilsson, K. Hansen, I. Schmidt, L. Vesterdal, P. Gundersen (2012)
Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient.The New phytologist, 194 1
J. Galloway, A. Townsend, J. Erisman, M. Bekunda, Z. Cai, J. Freney, L. Martinelli, S. Seitzinger, M. Sutton (2008)
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential SolutionsScience, 320
P. Thrall, M. Hochberg, J. Burdon, J. Bever (2007)
Coevolution of symbiotic mutualists and parasites in a community context.Trends in ecology & evolution, 22 3
P. Thrall, David Millsom, Alison Jeavons, M. Waayers, Geoffrey Harvey, D. Bagnall, J. Brockwell (2005)
Seed inoculation with effective root‐nodule bacteria enhances revegetation successJournal of Applied Ecology, 42
R. Denison (2000)
Legume Sanctions and the Evolution of Symbiotic Cooperation by RhizobiaThe American Naturalist, 156
C. Neuhauser, J. Fargione (2004)
A mutualism–parasitism continuum model and its application to plant–mycorrhizae interactionsEcological Modelling, 177
W. Schlesinger (2009)
On the fate of anthropogenic nitrogenProceedings of the National Academy of Sciences, 106
Joel Sachs, U. Mueller, T. Wilcox, J. Bull (2004)
The Evolution of CooperationThe Quarterly Review of Biology, 79
H. Gamper, U. Hartwig, A. Leuchtmann (2005)
Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure.The New phytologist, 167 2
N. Rabalais (2002)
Nitrogen in Aquatic Ecosystems, 31
M. Frederickson (2013)
Rethinking Mutualism Stability: Cheaters and the Evolution of SanctionsThe Quarterly Review of Biology, 88
Erol Akçay, E. Simms (2011)
Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium MutualismThe American Naturalist, 178
Hidetoshi Shimodaira, M. Hasegawa (1999)
Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic InferenceMolecular Biology and Evolution, 16
D. Bullock, Daniel Anderson (1998)
Evaluation of the Minolta SPAD-502 chlorophyll meter for nitrogen management in cornJournal of Plant Nutrition, 21
M. Gouy, Stéphane Guindon, O. Gascuel (2010)
SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building.Molecular biology and evolution, 27 2
R. Oono, R. Denison, E. Kiers (2009)
Controlling the reproductive fate of rhizobia: how universal are legume sanctions?The New phytologist, 183 4
Joel Sachs, S. Kembel, A. Lau, E. Simms (2009)
In Situ Phylogenetic Structure and Diversity of Wild Bradyrhizobium CommunitiesApplied and Environmental Microbiology, 75
N. Galtier, M. Gouy, C. Gautier (1996)
SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogenyComputer applications in the biosciences : CABIOS, 12 6
E. Kiers, Stuart West, R. Denison (2002)
Mediating mutualisms: farm management practices and evolutionary changes in symbiont co-operationJournal of Applied Ecology, 39
E. Simms, D. Taylor, Joshua Povich, Richard Shefferson, Joel Sachs, M. Urbina, Y. Tausczik (2006)
An empirical test of partner choice mechanisms in a wild legume–rhizobium interactionProceedings of the Royal Society B: Biological Sciences, 273
S. Elena, R. Lenski (2003)
Microbial genetics: Evolution experiments with microorganisms: the dynamics and genetic bases of adaptationNature Reviews Genetics, 4
Joel Sachs, J. Russell, A. Hollowell (2011)
Evolutionary Instability of Symbiotic Function in Bradyrhizobium japonicumPLoS ONE, 6
N. Johnson, G. Wilson, M. Bowker, J. Wilson, R. Miller, G. David, Tilman (2010)
Resource limitation is a driver of local adaptation in mycorrhizal symbiosesProceedings of the National Academy of Sciences, 107
R. Sterner, J. Elser (2002)
Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere
E. Kiers, R. Rousseau, S. West, R. Denison (2003)
Host sanctions and the legume–rhizobium mutualismNature, 425
J. Streeter, P. Wong (1988)
Inhibition of legume nodule formation and N2 fixation by nitrateCritical Reviews in Plant Sciences, 7
J. Wernegreen, M. Riley (1999)
Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages.Molecular biology and evolution, 16 1
Katy Heath, J. Stinchcombe (2014)
EXPLAINING MUTUALISM VARIATION: A NEW EVOLUTIONARY PARADOX?Evolution, 68
J. Galloway, F. Dentener, D. Capone, E. Boyer, R. Howarth, S. Seitzinger, G. Asner, C. Cleveland, P. Green, E. Holland, D. Karl, Anthony Michaels, J. Porter, A. Townsend, C. Vörösmarty (2004)
Nitrogen Cycles: Past, Present, and FutureBiogeochemistry, 70
D. Cusack, W. Silver, M. Torn, S. Burton, M. Firestone (2011)
Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests.Ecology, 92 3
J. Erisman, A. Bleeker, J. Galloway, M. Sutton (2007)
Reduced nitrogen in ecology and the environment.Environmental pollution, 150 1
S. West, E. Kiers, E. Simms, R. Denison (2002)
Sanctions and mutualism stability: why do rhizobia fix nitrogen?Proceedings of the Royal Society of London. Series B: Biological Sciences, 269
Robert May (1981)
The evolution of cooperationNature, 292
D. Six (2009)
Climate change and mutualismNature Reviews Microbiology, 7
E. Kiers, T. Palmer, A. Ives, J. Bruno, J. Bronstein (2010)
Mutualisms in a changing world: an evolutionary perspective.Ecology letters, 13 12
J. Halvorson, R. Black, Jeffrey Smith, E. Franz (1991)
Nitrogenase Activity, Growth and Carbon and Nitrogen Allocation in Wintergreen and Deciduous Lupin SeedlingsFunctional Ecology, 5
P. Vitousek, J. Aber, R. Howarth, G. Likens, P. Matson, D. Schindler, W. Schlesinger, D. Tilman (1997)
Technical Report: Human Alteration of the Global Nitrogen Cycle: Sources and ConsequencesEcological Applications, 7
Vitousek Vitousek, Aber Aber, Howarth Howarth, Likens Likens, Matson Matson, Schindler Schindler, Schlesinger Schlesinger, Tilman Tilman (1997)
Human alteration of the global nitrogen cycle: sources and consequencesEcol. App., 7
Katy Heath, P. Burke, J. Stinchcombe (2012)
Coevolutionary genetic variation in the legume‐rhizobium transcriptomeMolecular Ecology, 21
Joel Sachs, E. Simms (2006)
Pathways to mutualism breakdown.Trends in ecology & evolution, 21 10
Katy Heath, P. Tiffin (2009)
Stabilizing Mechanisms in a Legume-Rhizobium Mutualism, 63
R. Oono, Carolyn Anderson, R. Denison (2011)
Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonematesProceedings of the Royal Society B: Biological Sciences, 278
L. Moulin, G. Béna, C. Boivin-Masson, T. Stępkowski (2004)
Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus.Molecular phylogenetics and evolution, 30 3
R. Díaz, R. Rosenberg (2008)
Spreading Dead Zones and Consequences for Marine EcosystemsScience, 321
W. Ratcliff, Kyra Underbakke, R. Denison (2011)
Measuring the fitness of symbiotic rhizobiaSymbiosis, 55
E. Kiers, M. Hutton, R. Denison (2007)
Human selection and the relaxation of legume defences against ineffective rhizobiaProceedings of the Royal Society B: Biological Sciences, 274
R. Denison, E. Kiers (2004)
Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis.FEMS microbiology letters, 237 2
C. Cleveland, A. Townsend, D. Schimel, H. Fisher, R. Howarth, L. Hedin, S. Perakis, Erika Latty, J. Fischer, Adrien Elseroad, Matthew Wasson (1999)
Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystemsGlobal Biogeochemical Cycles, 13
D. Swofford, D. Swofford, D. Swofford (2002)
PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10
J. Swiader, A. Moore (2002)
SPAD-CHLOROPHYLL RESPONSE TO NITROGEN FERTILIZATION AND EVALUATION OF NITROGEN STATUS IN DRYLAND AND IRRIGATED PUMPKINS*Journal of Plant Nutrition, 25
S. Zechmeister-Boltenstern, K. Michel, M. Pfeffer (2011)
Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen depositionPlant and Soil, 343
Katy Heath, P. Tiffin (2007)
Context dependence in the coevolution of plant and rhizobial mutualistsProceedings of the Royal Society B: Biological Sciences, 274
S. F. Elena, R. E. Lenski (2003)
Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation, 4
T. Dickson, K. Gross (2013)
Plant community responses to long-term fertilization: changes in functional group abundance drive changes in species richnessOecologia, 173
S. Strauss, J. Lau, T. Schoener, P. Tiffin (2008)
Evolution in ecological field experiments: implications for effect size.Ecology letters, 11 3
C. Clark, D. Tilman (2008)
Loss of plant species after chronic low-level nitrogen deposition to prairie grasslandsNature, 451
Emily Grman, J. Lau, D. Schoolmaster, K. Gross (2010)
Mechanisms contributing to stability in ecosystem function depend on the environmental context.Ecology letters, 13 11
Stéphane Guindon, O. Gascuel (2003)
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Systematic biology, 52 5
N. Johnson (1993)
Can Fertilization of Soil Select Less Mutualistic Mycorrhizae?Ecological applications : a publication of the Ecological Society of America, 3 4
Human activities have altered the global nitrogen (N) cycle, and as a result, elevated N inputs are causing profound ecological changes in diverse ecosystems. The evolutionary consequences of this global change have been largely ignored even though elevated N inputs are predicted to cause mutualism breakdown and the evolution of decreased cooperation between resource mutualists. Using a long‐term (22 years) N‐addition experiment, we find that elevated N inputs have altered the legume–rhizobium mutualism (where rhizobial bacteria trade N in exchange for photosynthates from legumes), causing the evolution of less‐mutualistic rhizobia. Plants inoculated with rhizobium strains isolated from N‐fertilized treatments produced 17–30% less biomass and had reduced chlorophyll content compared to plants inoculated with strains from unfertilized control plots. Because the legume–rhizobium mutualism is the major contributor of naturally fixed N to terrestrial ecosystems, the evolution of less‐cooperative rhizobia may have important environmental consequences.
Evolution – Wiley
Published: Mar 1, 2015
Read and print from thousands of top scholarly journals.
Already have an account? Log in
Bookmark this article. You can see your Bookmarks on your DeepDyve Library.
To save an article, log in first, or sign up for a DeepDyve account if you don’t already have one.
Copy and paste the desired citation format or use the link below to download a file formatted for EndNote
Access the full text.
Sign up today, get DeepDyve free for 14 days.
All DeepDyve websites use cookies to improve your online experience. They were placed on your computer when you launched this website. You can change your cookie settings through your browser.