Biology Direct | |
What can ecosystems learn? Expanding evolutionary ecology with learning theory | |
Daniel A. Power6  Richard A. Watson5  Eörs Szathmáry3  Rob Mills1  Simon T. Powers4  C. Patrick Doncaster2  BłaŻej Czapp2  | |
[1] Department of Informatics, Faculty of Sciences, University of Lisbon, Lisbon, Portugal | |
[2] School of Biological Sciences, University of Southampton, Southampton, UK | |
[3] The Parmenides Found, Center for the Conceptual Foundations of Science, Pullach, Germany | |
[4] Department of Ecology & Evolution, University of Lausanne, Lausanne, Switzerland | |
[5] Institute for Life Sciences/Electronics and Computer Science, University of Southampton, Southampton, UK | |
[6] Electronics and Computer Science, University of Southampton, Southampton SO17 1BJ, UK | |
关键词: Community matrix; Regime shifts; Associative learning; Ecological memory; Network structures; Community assembly; Theoretical ecology; Lotka-Volterra dynamics; Alternative stable states; Evolutionary ecology; | |
Others : 1234986 DOI : 10.1186/s13062-015-0094-1 |
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received in 2015-04-08, accepted in 2015-10-26, 发布年份 2015 | |
【 摘 要 】
Background
The structure and organisation of ecological interactions within an ecosystem is modified by the evolution and coevolution of the individual species it contains. Understanding how historical conditions have shaped this architecture is vital for understanding system responses to change at scales from the microbial upwards. However, in the absence of a group selection process, the collective behaviours and ecosystem functions exhibited by the whole community cannot be organised or adapted in a Darwinian sense. A long-standing open question thus persists Are there alternative organising principles that enable us to understand and predict how the coevolution of the component species creates and maintains complex collective behaviours exhibited by the ecosystem as a whole?
Results
Here we answer this question by incorporating principles from connectionist learning, a previously unrelated discipline already using well-developed theories on how emergent behaviours arise in simple networks. Specifically, we show conditions where natural selection on ecological interactions is functionally equivalent to a simple type of connectionist learning, ‘unsupervised learning’, well-known in neural-network models of cognitive systems to produce many non-trivial collective behaviours. Accordingly, we find that a community can self-organise in a well-defined and non-trivial sense without selection at the community level; its organisation can be conditioned by past experience in the same sense as connectionist learning models habituate to stimuli. This conditioning drives the community to form a distributed ecological memory of multiple past states, causing the community to a) converge to these states from any random initial composition; b) accurately restore historical compositions from small fragments; c) recover a state composition following disturbance; and d) to correctly classify ambiguous initial compositions according to their similarity to learned compositions. We examine how the formation of alternative stable states alters the community’s response to changing environmental forcing, and we identify conditions under which the ecosystem exhibits hysteresis with potential for catastrophic regime shifts.
Conclusions
This work highlights the potential of connectionist theory to expand our understanding of evo-eco dynamics and collective ecological behaviours. Within this framework we find that, despite not being a Darwinian unit, ecological communities can behave like connectionist learning systems, creating internal conditions that habituate to past environmental conditions and actively recalling those conditions.
Reviewers
This article was reviewed by Prof. Ricard V Solé, Universitat Pompeu Fabra, Barcelona and Prof. Rob Knight, University of Colorado, Boulder.
【 授权许可】
2015 Power et al.
【 预 览 】
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【 参考文献 】
- [1]Levin SA: Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1998, 1(5):431-6.
- [2]Levin SA: Self-organization and the emergence of complexity in ecological systems. Bioscience 2005, 55(12):1075-9.
- [3]Anand M, Gonzalez A, Guichard F, Kolasa J, Parrott L: Ecological systems as complex systems: challenges for an emerging science. Diversity 2010, 2(3):395-410.
- [4]Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, et al.: A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 2006, 7(7):510-23.
- [5]Ulanowicz RE: Growth and Development: Ecosystems Phenomenology. Springer, New York, NY, USA; 1986.
- [6]Neill WE: The community matrix and interdependence of the competition coefficients. Am Nat. 1974, 108(962):399-408.
- [7]Proulx SR, Promislow DE, Phillips PC: Network thinking in ecology and evolution. Trends Ecol Evol 2005, 20(6):345-53.
- [8]Clements FE: Plant Succession: an Analysis of the Development of Vegetation vol. 242. Carnegie Institution of Washington, Washington, DC, USA; 1916.
- [9]Weiher E, Keddy P: Ecological Assembly Rules: Perspectives, Advances, Retreats. Cambridge University Press, Cambridge, UK; 2001.
- [10]Holling CS: Resilience and stability of ecological systems. Annu Rev Ecol Syst. 1973, 4:1-23.
- [11]Gallopín GC: Linkages between vulnerability, resilience, and adaptive capacity. Glob Environ Chang 2006, 16(3):293-303.
- [12]de Ruiter PC, Neutel AM, Moore JC: Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 1995, 269:1257-60.
- [13]Folke C: Resilience: the emergence of a perspective for social–ecological systems analyses. Glob Environ Chang 2006, 16(3):253-67.
- [14]Staniczenko P, Lewis OT, Jones NS, Reed-Tsochas F: Structural dynamics and robustness of food webs. Ecol Lett 2010, 13(7):891-9.
- [15]Higgins PA, Mastrandrea MD, Schneider SH: Dynamics of climate and ecosystem coupling: abrupt changes and multiple equilibria. Phil Trans R Soc London Series B Biol Sci. 2002, 357:647-56.
- [16]Cropp R, Gabric A: Ecosystem adaptation: Do ecosystems maximize resilience? Ecology 2002, 83(7):2019-26.
- [17]Beisner BE, Haydon DT, Cuddington K: Alternative stable states in ecology. Front Ecol Environ 2003, 1(7):376-82.
- [18]Scheffer M, Carpenter S, Foley JA, Folke C, Walker B: Catastrophic shifts in ecosystems. Nature 2001, 413(6856):591-6.
- [19]Lenton TM, van Oijen M: Gaia as a complex adaptive system. Phil Trans R Soc London Series B: Biol Sci 2002, 357(1421):683-95.
- [20]Ulanowicz RE: Aristotelean causalities in ecosystem development. Oikos 1990, 57(1):42-48.
- [21]Clarifying Gaia: regulation with or without natural selection. Scientists debate Gaia: the next century. MIT Press, Cambridge, Massachusetts; 2004.
- [22]Richardson JL: The organismic community: resilience of an embattled ecological concept. BioScience 1980, 30(7):465-71.
- [23]McIntosh RP: Ha gleason’s ‘individualistic concept’ and theory of animal communities: a continuing controversy. Biol Rev 1995, 70(2):317-57.
- [24]Levin SA: Evolution at the ecosystem level: On the evolution of ecosystem patterns. Contrib Sci 2011, 7(1):11-16.
- [25]Smith JM, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, et al.: Developmental constraints and evolution: a perspective from the mountain lake conference on development and evolution. Q Rev Biol. 1985, 60(3):265-87.
- [26]Gleason HA: The individualistic concept of the plant association. Bulletin Torrey Botanical Club 1926, 53(1):7-26.
- [27]Lawton JH: Are there general laws in ecology? Oikos 1999, 84(2):177-92.
- [28]Milne BT: Motivation and benefits of complex systems approaches in ecology. Ecosystems 1998, 1(5):449-56.
- [29]Thompson JN, Reichman O, Morin PJ, Polis GA, Power ME, Sterner RW, et al.: Frontiers of ecology. BioScience 2001, 51(1):15-24.
- [30]Matthews B, Narwani A, Hausch S, Nonaka E, Peter H, Yamamichi M, et al.: Toward an integration of evolutionary biology and ecosystem science. Ecol Lett 2011, 14(7):690-701.
- [31]Post DM, Palkovacs EP: Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Phil Trans R Soc B: Biol Sci 2009, 364(1523):1629-40.
- [32]Gross T, Sayama H: Adaptive Networks - Theory, Models and Applications. Springer, Germany; 2009.
- [33]Paperin G, Green DG, Sadedin S: Dual-phase evolution in complex adaptive systems. J R Soc Interface 2011, 8:609-29.
- [34]Schoener TW: The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 2011, 331(6016):426-9.
- [35]Turcotte MM, Reznick DN, Hare JD: The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecol Lett 2011, 14(11):1084-92.
- [36]Metz JA, Geritz SA, Meszéna G, Jacobs FJ, Van Heerwaarden JS: Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction. Stochastic Spatial Struct Dyn Syst 1996, 45:183-231.
- [37]Fussmann G, Loreau M, Abrams P: Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 2007, 21(3):465-77.
- [38]Harcombe W: Novel cooperation experimentally evolved between species. Evolution 2010, 64(7):2166-72.
- [39]Romano-Keeler J, Weitkamp JH: Maternal influences on fetal microbial colonization and immune development. Pediatr Res 2014, 77(1-2):189-95.
- [40]Faust K, Raes J: Microbial interactions: from networks to models. Nat Rev Microbiol 2012, 10(8):538-50.
- [41]Forslund K, Sunagawa S, Kultima JR, Mende DR, Arumugam M, Typas A, et al.: Country-specific antibiotic use practices impact the human gut resistome. Genome Res 2013, 23(7):1163-9.
- [42]David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al.: Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505(7484):559-63.
- [43]Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, et al.: Fundamentals of microbial community resistance and resilience. Front Microbiol. 2012, 3:417.
- [44]Case TJ, Holt RD, McPeek MA, Keitt TH: The community context of species’ borders: ecological and evolutionary perspectives. Oikos 2005, 108(1):28-46.
- [45]Mayr E: Wallace’s line in the light of recent zoogeographic studies. The Q Rev Biol 1944, 19(1):1-14.
- [46]Wallace AR: The Geographical Distribution of Animals: with a Study of the Relations of Living and Extinct Faunas as Elucidating the Past Changes of the Earth’s Surface vol. 1. Cambridge University Press, Cambridge, UK; 2011.
- [47]Angeler DG, Trigal C, Drakare S, Johnson RK, Goedkoop W: Identifying resilience mechanisms to recurrent ecosystem perturbations. Oecologia 2010, 164(1):231-41.
- [48]Carpenter SR, Ludwig D, Brock WA: Management of eutrophication for lakes subject to potentially irreversible change. Ecol Appl 1999, 9(3):751-71.
- [49]Hendry R, McGlade J: The role of memory in ecological systems. Proc R Soc Lond Ser B: Biol Sci 1995, 259(1355):153-9.
- [50]Peterson GD: Contagious disturbance, ecological memory, and the emergence of landscape pattern. Ecosystems 2002, 5(4):329-38.
- [51]Golinski M, Bauch C, Anand M: The effects of endogenous ecological memory on population stability and resilience in a variable environment. Ecol Model 2008, 212(3):334-41.
- [52]Brown WL, Wilson EO: Character displacement. Syst Zool 1956, 5(2):49-64.
- [53]Dayan T, Simberloff D: Ecological and community-wide character displacement: the next generation. Ecol Lett 2005, 8(8):875-94.
- [54]Thompson JN: The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, Il, USA; 2005.
- [55]McCulloch WS, Pitts W: A logical calculus of the ideas immanent in nervous activity. Bull Math Biophys 1943, 5(4):115-33.
- [56]Hinton GE, Sejnowski TJ: Unsupervised Learning: Foundations of Neural Computation. MIT Press, Cambridge, MA, USA; 1999.
- [57]Hopfield JJ: Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci 1982, 79(8):2554-8.
- [58]Watson RA, Buckley CL, Mills R: Optimisation in ‘self-modelling’ complex adaptive systems. Complexity 2010, 16(5):17-26.
- [59]Farmer JD: A rosetta stone for connectionism. Physica D: Nonlinear Phenomena 1990, 42(1):153-87.
- [60]Watson RA, Mills R, Buckley CL: Global adaptation in networks of selfish components: emergent associative memory at the system scale. Artif Life 2011, 17(3):147-66.
- [61]Mikhailov A, Mit’kov I, Sveshnikov N: Molecular associative memory. BioSystems 1990, 23(4):291-5.
- [62]Fernando CT, Liekens AM, Bingle LE, Beck C, Lenser T, Stekel DJ, et al.: Molecular circuits for associative learning in single-celled organisms. J R Soc Interface 2009, 6(34):463-9.
- [63]Vohradsky J: Neural model of the genetic network. J Biol Chem 2001, 276(39):36168-73.
- [64]Noonburg V: A neural network modeled by an adaptive lotka-volterra system. SIAM J Appl Math 1989, 49(6):1779-92.
- [65]Poderoso FC, Fontanari JF: Model ecosystem with variable interspecies interactions. J Phys A: Math Theoretical 2007, 40(30):8723.
- [66]Wilson DS: Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 1992, 73(6):1984-2000.
- [67]Watson RA, Wagner GP, Pavlicev M, Weinreich DM, Mills R: The evolution of phenotypic correlations and “developmental memory”. Evolution 2014, 68(4):1124-38.
- [68]Ackley DH, Hinton GE, Sejnowski TJ: A learning algorithm for boltzmann machines. Cogn Sci 1985, 9(1):147-69.
- [69]Hebb D: The Organization of Behavior; a Neuropsychological Theory. Wiley/Psychology Press, New York, NY, USA; 1949.
- [70]Ulanowicz RE: Utricularia’s secret: the advantage of positive feedback in oligotrophic environments. Eco Model 1995, 79(1):49-57.
- [71]Laland K, Odling-Smee J, Turner S: The role of internal and external constructive processes in evolution. J Physiol 2014, 592(11):2413-22.
- [72]Laland KN, Odling-Smee J, Feldman MW, Kendal J: Conceptual barriers to progress within evolutionary biology. Found Sci 2009, 14(3):195-216.
- [73]Gallardo B, Aldridge DC: Is great britain heading for a ponto–caspian invasional meltdown? J Appl Ecol 2015, 52(1):41-9.
- [74]Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, et al.: European buckthorn and asian soybean aphid as components of an extensive invasional meltdown in north america. Biol Invasions 2010, 12(9):2913-31.
- [75]Simberloff D, Von Holle B: Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1999, 1(1):21-32.
- [76]Hutchinson GE: The niche: an abstractly inhabited hypervolume. The ecological theatre and the evolutionary play. Yale University Press, New Haven, CT; 1965.
- [77]Wilson DS: The Natural Selection of Populations and Communities. Benjamin/Cummings Pub. Co., Menio Park, CA, USA; 1980.
- [78]Neher RA, Shraiman BI, Fisher DS: Rate of adaptation in large sexual populations. Genetics 2010, 184(2):467-81.
- [79]Weissman DB, Barton NH: Limits to the rate of adaptive substitution in sexual populations. PLoS Genet 2012, 8(6):1002740.
- [80]May RM: Some notes on estimating the competition matrix, α. Ecology 1975, 56(3):737-41.
- [81]Hughes JB, Roughgarden J: Aggregate community properties and the strength of species’ interactions. Proc Natl Acad Sci 1998, 95(12):6837-42.
- [82]Roughgarden J: Evolution of niche width. Am Nat. 1972, 106(952):683-718.
- [83]Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V, et al.: Early-warning signals for critical transitions. Nature 2009, 461(7260):53-9.
- [84]Dakos V, Scheffer M, van Nes EH, Brovkin V, Petoukhov V, Held H: Slowing down as an early warning signal for abrupt climate change. Proc Natl Acad Sci 2008, 105(38):14308-12.
- [85]Finn JT: Measures of ecosystem structure and function derived from analysis of flows. J Theor Biol 1976, 56(2):363-80.
- [86]Adams P: Hebb and darwin. J Theor Biol 1998, 195(4):419-38.
- [87]Fernando C, Szathmáry E, Husbands P: Selectionist and evolutionary approaches to brain function: a critical appraisal. Front Comput Neurosci. 2012, 6(24):0.
- [88]Betts RA, Lenton TM: Second chances for lucky gaia: a hypothesis of sequential selection. Gaia Circular 2008, 1(1):4-6.
- [89]Hopfield JJ, Tank DW: Computing with neural circuits- a model. Science 1986, 233(4764):625-33.
- [90]Law R, Morton RD: Permanence and the assembly of ecological communities. Ecology 1996, 77(3):762-75.
- [91]Roughgarden J: Theory of Population Genetics and Evolutionary Ecology: an Introduction. Macmillan, New York, NY, USA; 1979.