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Research articles
Evolution of nutrient acquisition: when adaptation fills the gap between contrasting ecological theories
Published:26 August 2010https://doi.org/10.1098/rspb.2010.1167
Abstract
Although plant strategies for acquiring nutrients have been widely studied from a functional point of view, their evolution is still not well understood. In this study, we investigate the evolutionary dynamics of these strategies and determine how they influence ecosystem properties. To do so, we use a simple nutrient-limited ecosystem model in which plant ability to take up nutrients is subject to adaptive dynamics. We postulate the existence of a trade-off between this ability and mortality. We show that contrasting strategies are possible as evolutionary outcomes, depending on the shape of the trade-off and, when nitrogen is considered as the limiting nutrient, on the intensity of symbiotic fixation. Our model enables us to bridge these evolutionary outcomes to classical ecological theories such as Hardin's tragedy of the commons and Tilman's rule of R*. Evolution does not systematically maximize plant biomass or primary productivity. On the other hand, each evolutionary outcome leads to a decrease in the availability of the limiting mineral nutrient, supporting the work of Tilman on competition between plants for a single resource. Our model shows that evolution can be used to link different classical ecological results and that adaptation may influence ecosystem properties in contrasted ways.
References
- 1
Fussmann G. F., Loreau M.& Abrams P. A. . 2007 Eco-evolutionary dynamics of communities and ecosystems. Funct. Ecol. 21, 465–477.doi:10.1111/j.1365-2435.2007.01275.x (doi:10.1111/j.1365-2435.2007.01275.x). Crossref, Web of Science, Google Scholar - 2
Johnson M. T. J.& Stinchcombe J. R. . 2007 An emerging synthesis between community ecology and evolutionary biology. Trends Ecol. Evol. 22, 250–257.doi:10.1016/j.tree.2007.01.014 (doi:10.1016/j.tree.2007.01.014). Crossref, PubMed, Web of Science, Google Scholar - 3
Urban M. C., 2008 The evolutionary ecology of metacommunities. Trends Ecol. Evol. 23, 311–317.doi:10.1016/j.tree.2008.02.007 (doi:10.1016/j.tree.2008.02.007). Crossref, PubMed, Web of Science, Google Scholar - 4
Kylafis G.& Loreau M. . 2008 Ecological and evolutionary consequences of niche construction for its agent. Ecol. Lett. 11, 1072–1081.doi:10.1111/j.1461-0248.2008.01220.x (doi:10.1111/j.1461-0248.2008.01220.x). Crossref, PubMed, Web of Science, Google Scholar - 5
Menge D. N. L., Levin S. A.& Hedin L. O. . 2008 Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation. Proc. Natl Acad. Sci. USA 105, 1573–1578.doi:10.1073/pnas.0711411105 (doi:10.1073/pnas.0711411105). Crossref, PubMed, Web of Science, Google Scholar - 6
Menge D. N. L.& Weitz J. S. . 2009 Dangerous nutrients: evolution of phytoplankton resource uptake subject to virus attack. J. Theor. Biol. 257, 104–115.doi:10.1016/j.jtbi.2008.10.032 (doi:10.1016/j.jtbi.2008.10.032). Crossref, PubMed, Web of Science, Google Scholar - 7
de Mazancourt C., Loreau M.& Abbadie L. . 1998 Grazing optimization and nutrient cycling: when do herbivores enhance plant production? Ecology 79, 2242–2252.doi:10.1890/0012-9658(1998)079[2242:GOANCW]2.0.CO;2 (doi:10.1890/0012-9658(1998)079[2242:GOANCW]2.0.CO;2). Crossref, Web of Science, Google Scholar - 8
Barot S., Ugolini A.& Brikci F. B. . 2007 Nutrient cycling efficiency explains the long-term effect of ecosystem engineers on primary production. Funct. Ecol. 21, 1–10. Crossref, Web of Science, Google Scholar - 9
Boudsocq S., Lata J. C., Mathieu J., Abbadie L.& Barot S. . 2009 Modelling approach to analyse the effects of nitrification inhibition on primary production. Funct. Ecol. 23, 220–230.doi:10.1111/j.1365-2435.2008.01476.x (doi:10.1111/j.1365-2435.2008.01476.x). Crossref, Web of Science, Google Scholar - 10
Jones C. G., Lawton J. H.& Shachack M. . 1994 Organisms as ecosystem engineers. Oikos 69, 373–386.doi:10.2307/3545850 (doi:10.2307/3545850). Crossref, Web of Science, Google Scholar - 11
Jones C. G., Lawton J. H.& Shachak M. . 1997 Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946–1957.doi:10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2 (doi:10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2). Crossref, Web of Science, Google Scholar - 12
Loeuille N., Loreau M.& Ferrière R. . 2002 Consequences of plant-herbivore coevolution on the dynamics and functioning of ecosystems. J. Theor. Biol. 217, 369–381.doi:10.1006/jtbi.2002.3032 (doi:10.1006/jtbi.2002.3032). Crossref, PubMed, Web of Science, Google Scholar - 13
Odling-Smee F. J., Laland K. N.& Feldman M. W. . 2003 Niche construction: the neglected process in evolution. Princeton, NJ: Princeton University Press. Google Scholar - 14
Loeuille N.& Loreau M. . 2004 Nutrient enrichment and food chains: can evolution buffer top-down control? Theor. Popul. Biol. 65, 285–298.doi:10.1016/j.tpb.2003.12.004 (doi:10.1016/j.tpb.2003.12.004). Crossref, PubMed, Web of Science, Google Scholar - 15
Odum E. P. . 1969 The strategy of ecosystem development. Science 164, 262–270.doi:10.1126/science.164.3877.262 (doi:10.1126/science.164.3877.262). Crossref, PubMed, Web of Science, Google Scholar - 16
Loreau M. . 1998 Ecosystem development explained by competition within and between material cycles. Proc. R. Soc. Lond. B 265, 33–38.doi:10.1098/rspb.1998.0260 (doi:10.1098/rspb.1998.0260). Link, Web of Science, Google Scholar - 17
Simms E. L.& Rausher M. D. . 1987 Costs and benefits of plant resistance to herbivory. Am. Nat. 130, 570–581.doi:10.1086/284731 (doi:10.1086/284731). Crossref, Web of Science, Google Scholar - 18
Van der Meijden E., Wijn M.& Verkaar H. J. . 1988 Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51, 355–363.doi:10.2307/3565318 (doi:10.2307/3565318). Crossref, Web of Science, Google Scholar - 19
Herms D. A.& Mattson W. J. . 1992 The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283–335.doi:10.1086/417659 (doi:10.1086/417659). Crossref, Web of Science, Google Scholar - 20
Mauricio R. . 1998 Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am. Nat. 151, 20–28.doi:10.1086/286099 (doi:10.1086/286099). Crossref, PubMed, Web of Science, Google Scholar - 21
Hobbie S. E. . 1992 Effects of plant species on nutrient cycling. Trends Ecol. Evol. 7, 336–339.doi:10.1016/0169-5347(92)90126-V (doi:10.1016/0169-5347(92)90126-V). Crossref, PubMed, Web of Science, Google Scholar - 22
Hardin G. . 1968 The tragedy of the commons. Science 162, 1243–1248.doi:10.1126/science.162.3859.1243 (doi:10.1126/science.162.3859.1243). Crossref, PubMed, Web of Science, Google Scholar - 23
Tilman D. . 1982 Resource competition and community structure. Princeton, NJ: Princeton University Press. Google Scholar - 24
Rankin D. J., Bargum K.& Kokko H. . 2007 The tragedy of the commons in evolutionary biology. Trends Ecol. Evol. 22, 643–651.doi:10.1016/j.tree.2007.07.009 (doi:10.1016/j.tree.2007.07.009). Crossref, PubMed, Web of Science, Google Scholar - 25
Metz J. A. J., Nisbet R. M.& Geritz S. A. H. . 1992 How should we define ‘fitness’ for general ecological scenarios? Trends Ecol. Evol. 7, 198–202.doi:10.1016/0169-5347(92)90073-K (doi:10.1016/0169-5347(92)90073-K). Crossref, PubMed, Web of Science, Google Scholar - 26
Dieckmann U.& Law R. . 1996 The dynamical theory of coevolution: a derivation from stochastic ecological processes. J. Math. Biol. 34, 579–612.doi:10.1007/BF02409751 (doi:10.1007/BF02409751). Crossref, PubMed, Web of Science, Google Scholar - 27
Dieckmann U. . 1997 Can adaptive dynamics invade? Trends Ecol. Evol. 12, 128–131.doi:10.1016/S0169-5347(97)01004-5 (doi:10.1016/S0169-5347(97)01004-5). Crossref, PubMed, Web of Science, Google Scholar - 28
Raison R. J. . 1979 Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant Soil 51, 73–108.doi:10.1007/BF02205929 (doi:10.1007/BF02205929). Crossref, Web of Science, Google Scholar - 29
Bowman D. M. J. S., 2009 Fire in the earth system. Science 324, 481–484.doi:10.1126/science.1163886 (doi:10.1126/science.1163886). Crossref, PubMed, Web of Science, Google Scholar - 30
May R. M. . 1974 Stability and complexity in model ecosystems. Princeton, NJ: Princeton University Press. Google Scholar - 31
Metz J. A. J., Geritz S. A. H., Meszéna G., Jacobs F. J. A.& Van Heervaarden J. S. . 1996 Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction. Stochastic and spatial structures of dynamical systems (eds, Van Strien S. J.& Verduyn S. M. ), pp. 183–231. Amsterdam, The Netherlands: Lunel, KNAM Verhandlingen. Google Scholar - 32
Geritz S. A. H., Metz J. A. J., Kisdi E.& Meszena G. . 1997 Dynamics of adaptation and evolutionary branching. Phys. Rev. Lett. 78, 2024–2027.doi:10.1103/PhysRevLett.78.2024 (doi:10.1103/PhysRevLett.78.2024). Crossref, Web of Science, Google Scholar - 33
Marrow P., Dieckmann U.& Law R. . 1996 Evolutionary dynamics of predator–prey systems: an ecological perspective. J. Math. Biol. 34, 556–578.doi:10.1007/BF02409750 (doi:10.1007/BF02409750). Crossref, PubMed, Web of Science, Google Scholar - 34
Geritz S. A. H., Kisdi E., Meszéna G.& Metz J. A. J. . 1998 Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol. 12, 35–57.doi:10.1023/A:1006554906681 (doi:10.1023/A:1006554906681). Crossref, Web of Science, Google Scholar - 35
Eshel I. . 1983 Evolutionary and continuous stability. J. Theor. Biol. 103, 99–111.doi:10.1016/0022-5193(83)90201-1 (doi:10.1016/0022-5193(83)90201-1). Crossref, Web of Science, Google Scholar - 36
Matsuda H.& Abrams P. A. . 1994 Runaway evolution to self-extinction under asymmetrical competition. Evolution 48, 1764–1772.doi:10.2307/2410506 (doi:10.2307/2410506). Crossref, PubMed, Web of Science, Google Scholar - 37
Parvinen K. . 2005 Evolutionary suicide. Acta Biotheor. 53, 241–264.doi:10.1007/s10441-005-2531-5 (doi:10.1007/s10441-005-2531-5). Crossref, PubMed, Web of Science, Google Scholar - 38
Rankin D. J.& López-Sepulcre A. . 2005 Can adaptation lead to extinction? Oikos 111, 616–619. Crossref, Web of Science, Google Scholar - 39
Crews T. E. . 1999 The presence of nitrogen fixing legumes in terrestrial communities: evolutionary versus ecological considerations. Biogeochemistry 46, 233–246. Crossref, Web of Science, Google Scholar - 40
Rastetter E. B., Vitousek P. M., Field C., Shaver G. R., Herbert D.& Gren G. I. . 2001 Resource optimization and symbiotic nitrogen fixation. Ecosystems 4, 369–388.doi:10.1007/s10021-001-0018-z (doi:10.1007/s10021-001-0018-z). Crossref, Web of Science, Google Scholar - 41
Vitousek P. M., 2002 Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45.doi:10.1023/A:1015798428743 (doi:10.1023/A:1015798428743). Crossref, Web of Science, Google Scholar - 42
Knops J. M. H., Bradley K. L.& Wedin D. . 2002 Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol. Lett. 5, 454–466.doi:10.1046/j.1461-0248.2002.00332.x (doi:10.1046/j.1461-0248.2002.00332.x). Crossref, Web of Science, Google Scholar - 43
Raynaud X., Lata J. C.& Leadley P. . 2006 Soil microbial loop and nutrient uptake by plants: a test using a coupled C : N model of plant–microbial interactions. Plant Soil 287, 95–116.doi:10.1007/s11104-006-9003-9 (doi:10.1007/s11104-006-9003-9). Crossref, Web of Science, Google Scholar - 44
Dijkstra F. A.& Cheng W. . 2007 Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecol. Lett. 10, 1046–1053.doi:10.1111/j.1461-0248.2007.01095.x (doi:10.1111/j.1461-0248.2007.01095.x). Crossref, PubMed, Web of Science, Google Scholar
