Phenotypic variability promotes diversity and stability in competitive communities.
Intraspecific variation
Lotka-Volterra dynamics
coexistence
network theory
replicator dynamics
Journal
Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949
Informations de publication
Date de publication:
Nov 2019
Nov 2019
Historique:
received:
25
02
2019
revised:
08
04
2019
revised:
19
06
2019
accepted:
03
07
2019
pubmed:
3
8
2019
medline:
18
10
2019
entrez:
3
8
2019
Statut:
ppublish
Résumé
Intraspecific variation is at the core of evolutionary theory, and yet, from an ecological perspective, we have few robust expectations for how this variation should affect the dynamics of large communities. Here, by adapting an approach from evolutionary game theory, we show that the incorporation of phenotypic variability into competitive networks dramatically alters the dynamics across ecological timescales, stabilising the systems and buffering the communities against demographic perturbations. The beneficial effects of phenotypic variability are strongest when there are substantial differences among phenotypes and when phenotypes are inherited with moderately high fidelity; yet even low levels of variation lead to significant increases in diversity, stability, and robustness. By identifying a simple and ubiquitous stabilising force in competitive communities, this work contributes to our core understanding of how biological diversity is maintained in natural systems.
Types de publication
Letter
Langues
eng
Sous-ensembles de citation
IM
Pagination
1776-1786Subventions
Organisme : Division of Environmental Biology
ID : 1148867
Organisme : Universidad Politécnica de Madrid. Programa Propio - Movilidad
Organisme : Human Frontier Science Program
Organisme : Spanish Ministerio de Economı́a y Competitividad
ID : CGL2015-69034-P
Informations de copyright
© 2019 John Wiley & Sons Ltd/CNRS.
Références
Achouak, W., Conrod, S., Cohen, V. & Heulin, T. (2004). Phenotypic variation of Pseudomonas brassicacearum as a plant root-colonization strategy. Mol. Plant Microbe Interact., 17, 872-879.
Ackleh, A. & Hu, S. (2007). Comparison between stochastic and deterministic selection-mutation models. Math. Biosci. Eng., 4(2), 133-157.
Ackleh, A.S., Ma, B. & Salceanu, P.L. (2011). Persistence and global stability in a selection-mutation size-structured model. J. Biol. Dyn., 5, 436-453.
Ackleh, A.S., Sacker, R.J. & Salceanu, P. (2014). On a discrete selection-mutation model. J. Diff. Eq. Appl., 20, 1383-1403.
Agrawal, A.A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science, 294, 321-326.
Aguirre, J.D. & Marshall, D.J. (2012). Genetic diversity increases population productivity in a sessile marine invertebrate. Ecology, 93, 1134-1142.
Allesina, S. & Levine, J.M. (2011). A competitive network theory of species diversity. Proc. Natl Acad. Sci., 108, 5638-5642.
Antal, T., Traulsen, A., Ohtsuki, H., Tarnita, C.E. & Nowak, M.A. (2009). Mutation-selection equilibrium in games with mixed strategies. J. Theor. Biol., 261, 50-57.
Auld, J.R., Agrawal, A.A. & Relyea, R.A. (2010). Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. B Biol. Sci., 277, 503-511.
Ausubel, E.D. & Frederick, M. (2002). Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature, 416, 740-743.
Barabás, G. & D'Andrea, R. (2016). The effect of intraspecific variation and heritability on community pattern and robustness. Ecol. Lett., 19, 977-986.
Baym, M., Lieberman, T.D., Kelsic, E.D., Chait, R., Gross, R., Yelin, I. & et al (2016). Spatiotemporal microbial evolution on antibiotic landscapes. Science, 353(6304), 1147-1151.
Boddy, L. (2000). Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol., 31, 185-194.
Bomze, I.M. & Burger, R. (1995). Stability by mutation in evolutionary games. Games Econ. Behav., 11(2), 146-172.
Brandl, F. (2017). The distribution of optimal strategies in symmetric zero-sum games. Games Econ. Behav., 104, 674-680.
Bürger, R. (1998). Mathematical properties of mutation-selection models. Genetica, 102(103), 279-298.
Buss, L.W. & Jackson, J.B.C. (1979). Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat., 113, 223-234.
Carja, O. & Plotkin, J.B. (2017). The evolutionary advantage of heritable phenotypic heterogeneity. Sci. Rep., 7, 1-12.
Carrara, F., Giometto, A., Seymour, M., Rinaldo, A. & Altermatt, F. (2015). Inferring species interactions in ecological communities: a comparison of methods at different levels of complexity. Methods Ecol. Evol., 6, 895-906.
Caswell, H. (2001). Matrix Population Models. Sinauer Associates, Sunderland, MA.
Chawanya, T. & Tokita, K. (2002). Large-dimensional replicator equations with antisymmetric random interactions. J. Phys. Soc. Jpn., 71, 429-431.
Chesson, P. (2000). Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst., 31, 343-366.
Condit, R., Chisholm, R.A. & Hubbell, S.P. (2012). Thirty years of forest census at Barro Colorado and the importance of immigration in maintaining diversity. PLoS ONE, 7, 1-6.
Crowther, T.W., Maynard, D.S., Crowther, T., Peccia, J., Smith, J. & Bradford, M.A. (2014). Untangling the fungal niche: the trait-based approach. Frontiers in Microbiology, 5, 1-12.
Dawson, T.P., Jackson, S.T., House, J.I., Prentice, I.C. & Mace, G.M. (2011). Beyond predictions: biodiversity conservation in a changing climate. Science, 332, 53-58.
DeAngelis, D.L. (2013). Intraspecific trait variation and its effects on food chains. Math. Biosci., 244, 91-97.
Des Roches, S., Post, D.M., Turley, N.E., Bailey, J.K., Hendry, A.P., Kinnison, M.T. et al. (2018). The ecological importance of intraspecific variation. Nat. Ecol. Evol., 2, 57-64.
Fisher, D.C. & Reeves, R.B. (1995). Optimal strategies for random tournament games. Linear Algebra Appl., 217, 83-85.
Fisher, D.C. & Ryan, J. (1992). Optimal strategies for a generalized ‘Scissors, Paper, and Stone’ game. Am. Math. Monthly, 99, 935-942.
Fontana, S., Thomas, M.K., Moldoveanu, M., Spaak, P. & Pomati, F. (2018). Individual-level trait diversity predicts phytoplankton community properties better than species richness or evenness. ISME J., 12, 356-366.
Forsman, A. & Wennersten, L. (2016). Inter-individual variation promotes ecological success of populations and species: evidence from experimental and comparative studies. Ecography, 39, 630-648.
Gafiychuk, V.V. (2004). Replicator - mutator evolutionary dynamics. J. Nonlinear Math. Phy., 11, 350-360.
Gasch, A.P. (2007). Comparative genomics of the environmental stress response in ascomycete fungi. Yeast, 24, 961-976.
Gibert, J.P. & DeLong, J.P. (2017). Phenotypic variation explains food web structural patterns. Proc. Natl Acad. Sci., 114(42), 11187-11192.
Gluckman, P.D., Lillycrop, K.A., Vickers, M.H., Pleasants, A.B., Phillips, E.S., Beedle, A.S. et al. (2007). Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc. Natl Acad. Sci., 104, 12796-800.
Grilli, J., Barabas, G., Michalska-smith, M.J. & Allesina, S. (2017). Higher-order interactions stabilize dynamics in competitive network models. Nature, 548, 210-213.
Hadeler, K.P. (1981). Stable polymorphisms in a selection model with mutation. SIAM J. Appl. Math., 41, 1-7.
Hart, S.P., Schreiber, S.J. & Levine, J.M. (2016). How variation between individuals affects species coexistence. Ecol. Lett., 19, 825-836.
Hart, S.P., Turcotte, M.M. & Levine, J.M. (2019). Effects of rapid evolution on species coexistence. Proc. Natl Acad. Sci., 116, 2112-2117.
Hofbauer, J. (1985). The selection mutation equation. J. Math. Biol., 23, 41-53.
Hofbauer, J., Schuster, P. & Sigmund, K. (1979). A note on evolutionary stable strategies and game dynamics. J. Theor. Biol., 81, 609-612.
Izquierdo, S.S. & Izquierdo, L.R. (2011). Strictly dominated strategies in the replicator-mutator dynamics. Games, 2, 355-364.
Kerr, B., Riley, M.A., Feldman, M.W. & Bohannan, B.J.M. (2002). Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature, 418, 171-174.
Kingman, J.F.C. (1961). A mathematical problem in population genetics. Proc. Camb. Philos. Soc., 57, 574-582.
Komarova, N.L. (2004). Replicator-mutator equation, universality property and population dynamics of learning. J. Theor. Biol., 230, 227-239.
Maynard, D.S., Bradford, M.A., Lindner, D.L., van Diepen, L.T.A., Frey, S.D., Crowther, T.W. et al. (2017). Diversity begets diversity in competition for space. Nat. Ecol. Evol., 1, 0156.
Maynard, D.S., Wootton, J.T., Serván, C.A. & Allesina, S. (2019). Reconciling empirical interactions and species coexistence. Ecol. Lett., 22, 1028-1037.
Nahum, J.R., Harding, B.N. & Kerr, B. (2011). Evolution of restraint in a structured rock-paper-scissors community. Proc. Natl Acad. Sci., 108, 10831-10838.
Nakayama, H., Sinha, N.R. & Kimura, S. (2017). How do plants and phytohormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues. Front. Plant Sci., 8, 1-7.
Neubert, M.G. & Caswell, H. (1997). Alternatives to resilience for measuring the responses of ecological systems to perturbations. Ecology, 78, 653-665.
Nicotra, A., Atkin, O.K., Bonser, S.P., Davidson, A., Finnegan, E.J., Mathesius, U. et al. (2010). Plant phenotypic plasticity in a changing climate. Trends Plant Sci., 15, 684-92.
Owens, I.P.F. & Hartley, I.R. (1998). Sexual dimorphism in birds:why are there so many forms of dimorphism? Proc. R. Soc. B Biol. Sci., 265, 397-407.
Petraitis, P.S. (1979). Competitive networks and measures of intransivity. Am. Nat., 114, 921-925.
Reichenbach, T., Mobilia, M. & Frey, E. (2007). Mobility promotes and jeopardizes biodiversity in rock-paper-scissors games. Nature, 448, 1046-1049.
Remy, J.-J. (2010). Stable inheritance of an acquired behavior in Caenorhabditis elegans. Curr. Biol., 20, R877-R878.
Sampedro, L., Moreira, X. & Zas, R. (2011). Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J. Ecol., 99, 818-827.
Sauer, K., Camper, A.K., Ehrlich, G.D., William, J. & Davies, D.G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofil. J. Bacteriol., 184, 1140-1154.
Schlichting, C.D. & Smith, H. (2002). Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes. Evol. Ecol., 16, 189-211.
Schmidt, B.R., Ramer, N. & Van Buskirk, J. (2006). A trophic polymorphism induced by both predators and prey. Evol. Ecol. Res., 8, 1301-1309.
Schreiber, S.J. & Killingback, T.P. (2013). Spatial heterogeneity promotes coexistence of rock-paper-scissors metacommunities. Theor. Popul. Biol., 86, 1-11.
Schreiber, S.J., Bürger, R. & Bolnick, D.I. (2011). The community effects of phenotypic and genetic variation within a predator population. Ecology, 92, 1582-1593.
Simpson, S.S.J., Sword, G.A.G. & Lo, N. (2011). Polyphenism in insects. Curr. Biol., 21, R738-R749.
Stadler, P.F. & Schuster, P. (1992). Mutation in autocatalytic reaction networks. J. Math. Biol., 30, 597-632.
Sultan, S.E. (2000). Phenotypic plasticity for plant development, function and life history. Trends Plant Sci., 5, 537-542.
Turcotte, M.M. & Levine, J.M. (2016). Phenotypic plasticity and species coexistence. Trends Ecol. Evol., 31, 803-813.
Turelli, M. & Barton, N.H. (1994). Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics, 138, 913-941.
Veening, J.-W., Smits, W.K. & Kuipers, O.P. (2008a). Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol., 62, 193-210.
Veening, J.-W., Stewart, E.J., Berngruber, T.W., Taddei, F., Kuipers, O.P. & Hamoen, L.W. (2008b). Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl Acad. Sci. U. S. A., 105, 4393-4398.
Vellend, M. (2006). The consequences of genetic diversity in competitive communities. Ecology, 87, 304-311.
Violle, C., Enquist, B.J., McGill, B.J., Jiang, L., Albert, C.H., Hulshof, C. et al. (2012). The return of the variance: intraspecific variability in community ecology. Trends Ecol. Evol., 27, 244-252.
Whitman, D. & Agrawal, A. (2009). What is phenotypic plasticity and why is it important? In: Phenotypic Plasticity of Insects: Mechanisms and Consequences (eds Whitman, D.W. & Ananthakrishnan, T.N.). Science Publishers, Enfield, pp. 1-63.
Wimberger, P.H. (1994). Trophic polymorphisms, plasticity, and speciation in vertebrates. In: Theory and application in fish feeding ecology (eds Stouder, D., Fresh, K. & Feller, R.). University of South Carolina Press, Columbia, SC, pp. 19-43.
Yamauchi, A. & Miki, T. (2009). Intraspecific niche flexibility facilitates species coexistence in a competitive community with a fluctuating environment. Oikos, 118, 55-66.
Zhang, Y.Y., Fischer, M., Colot, V. & Bossdorf, O. (2013). Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol., 197, 314-322.