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Biology & Philosophy

, 34:3 | Cite as

Does God roll dice? Neutrality and determinism in evolutionary ecology

  • Som B. Ale
  • Abdel Halloway
  • William A. Mitchell
  • Christopher J. Whelan
Area Review

Abstract

A tension between perspectives that emphasize deterministic versus stochastic processes has sparked controversy in ecology since pre-Darwinian times. The most recent manifestation of the contrasting perspectives arose with Hubbell’s proposed “neutral theory”, which hypothesizes a paramount role for stochasticity in ecological community composition. Here we shall refer to the deterministic and the stochastic perspectives as the niche-based and neutral-based research programs, respectively. Our goal is to represent these perspectives in the context of Lakatos’ notion of a scientific research program. We argue that the niche-based program exhibits all the characteristics of a robust, progressive research program, including the ability to deal with disconfirming data by generating new testable predictions within the program. In contrast, the neutral-based program succeeds as a mathematical tool to capture, as epiphenomena, broad-scale patterns of ecological communities but appears to handle disconfirming data by incorporating hypotheses and assumptions from outside the program, specifically, from the niche-based program. We conclude that the neutral research program fits the Lakatosian characterization of a degenerate research program.

Keywords

Determinism Neutral theory Niche theory Scientific research program Stochasticity 

Notes

Acknowledgements

Thanks are due to D. W. Morris for intellectual discussions when Som B. Ale was at Lakehead University with support from Canada’s International Polar Year program “Arctic Wildlife Observatories Linking Vulnerable EcoSystems” and Canada’ Natural Sciences and Engineering Research Council. The authors also thank Burt Kotler, an anonymous reviewer, and Linus Svensson for crisp comments on a previous draft of the manuscript. Abdel Halloway wishes to thank the National Science Foundation (NSF) Graduate Research Fellowship (DGE-0907994 and DGE-1444315) for support. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors(s).

Glossary

Dispersal limitation

Limitation of distribution or abundance in the vicinity of its parents because of either constraints on dispersal or inadequate production of dispersing individuals.

Ecological drift

Under ecological drift (Hubbell 2001) all individuals in the community, regardless of species, have equal probabilities of giving birth, dying, immigrating to another location, and (in one version of the model) acquiring a mutation that will eventually result in speciation. This does not mean that all species have an equal chance. Abundant species have a greater likelihood of being drawn, but only by virtue of their abundance. Individuals are equal, but species, as collective entities, are not (Norris 2003)

Ecological equivalence

when differences among individuals belonging to different species do not translate into differences in their probabilities of beingand persisting, in the present and future community

Neutrality equivalence, and symmetry

That different individuals from different species belonging to the same functionally uniform ecological community have similar birth, death and dispersal rates (Hubbell 2001; Etienne and Olff 2005). The neutrality hypothesis is that differences in species traits do not either affect the chances of that species being present or absent in a community, or influence changes in their relative abundances

Niche theory

Species can stably coexist in an ecological community if their characteristics (or traits) allow them to specialize on one particular set of resources or environment conditions (niches) in which they are superior to their competitors (Grinnell 1917; Hutchinson 1957; Chase and Leibold 2003)

Relative species abundance

The probability that a species has n individuals in a given region. When multiplied by the total number of species in the region this gives the number of species with n individuals. This is known as the species-abundance distribution

References

  1. Allesina S, Tang S (2012) Stability criteria for complex ecosystems. Nature 483:205–208CrossRefGoogle Scholar
  2. Allouche O, Kalyuzhny M, Moreno-Rueda G, Pizarro M, Kadmon R (2012) Area–heterogeneity trade-off and the diversity of ecological communities. Proc Natl Acad Sci USA 109:17495–17500CrossRefGoogle Scholar
  3. Alonso D, Etienne RS, McKane AJ (2006) The merits of neutral theory. TREE 21:451–457Google Scholar
  4. Azaele S, Suweis S, Grilli J, Volkov I, Banavar JR, Maritan A (2016) Statistical mechanics of ecological systems: neutral theory and beyond. Rev Mod Phys 88:035003.  https://doi.org/10.1103/RevModPhys.88.035003 CrossRefGoogle Scholar
  5. Bell G (2000) The distribution of abundance in neutral communities. Am Nat 155:606–617CrossRefGoogle Scholar
  6. Bell G (2001) Neutral macroecology. Science 293:2413–2418CrossRefGoogle Scholar
  7. Brown JH (1995) Macroecology. University of Chicago Press, ChicagoGoogle Scholar
  8. Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation-risk. Evol Ecol Res 1:49–71Google Scholar
  9. Brown JS (2001) Ngongas and ecology: on having a worldview. Oikos 94:6–16CrossRefGoogle Scholar
  10. Brown JS (2016) Why Darwin would have loved evolutionary game theory. Proc R Soc Lond B Biol Sci 283:20160847.  https://doi.org/10.1098/rspb.2016.0847 CrossRefGoogle Scholar
  11. Bunin G (2017) Ecological communities with Lotka–Volterra dynamics. Phys Rev E 95:042414.  https://doi.org/10.1103/PhysRevE.95.042414 CrossRefGoogle Scholar
  12. Caswell H (1976) Community structure: a neutral model analysis. Ecol Monogr 46:327–354CrossRefGoogle Scholar
  13. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  14. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Evol Syst 31:343–366CrossRefGoogle Scholar
  15. Clark JS (2009) Beyond neutral science. TREE 24:8–15Google Scholar
  16. Clark JS (2012) The coherence problem with the Unified Neutral theory of biodiversity. TREE 27:198–202Google Scholar
  17. Clements FE (1916) Plant succession: an analysis of the development of vegetation. Carnegie Institute of Washington Publication, WashingtonCrossRefGoogle Scholar
  18. Connor EF, Simberloff DS (1979) The assembly of species communities: chance or competition? Ecology 60:1132–1140CrossRefGoogle Scholar
  19. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. J. Murray, LondonCrossRefGoogle Scholar
  20. Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Cambridge, Belknap, pp 342–444Google Scholar
  21. Elton CS (1927) Animal ecology. Sidgwick and Jackson, LondonGoogle Scholar
  22. Etienne RS, Olff H (2005) Bayesian analysis of species abundance data: assessing the relative importance of dispersal and niche-partitioning for the maintenance of biodiversity. Ecol Lett 8:493–504CrossRefGoogle Scholar
  23. Etienne RS, Apol MEF, Olff H, Weissing FJ (2007) Modes of speciation and the neutral theory of biodiversity. Oikos 116:241–258CrossRefGoogle Scholar
  24. Fisher CK, Mehta P (2014) The transition between the niche and neutral regimes in ecology. Proc Natl Acad Sci USA 111:13111–13116CrossRefGoogle Scholar
  25. Fretwell SD, Lucas HL Jr (1969) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 14:16–36CrossRefGoogle Scholar
  26. Gewin V (2006) Beyond neutrality—ecology finds its niche. PLoS Biol 4:e278CrossRefGoogle Scholar
  27. Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53:7–26CrossRefGoogle Scholar
  28. Gotelli NJ, McGill BJ (2006) Null versus neutral models: what’s the difference? Ecography 29:793–800CrossRefGoogle Scholar
  29. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409CrossRefGoogle Scholar
  30. Grinnell J (1917) Field tests of theories concerning distributional control. Am Nat 51:115–128CrossRefGoogle Scholar
  31. Haegeman B, Etienne RS (2008) Relaxing the zero-sum assumption in neutral biodiversity theory. J Theor Biol 252:288–294CrossRefGoogle Scholar
  32. Halley JM, Iwasa Y (2011) Neutral theory as a predictor of avifaunal extinctions after habitat loss. Proc Natl Acad Sci USA 108:2316–2321CrossRefGoogle Scholar
  33. Harte J (2003) Tail of death and resurrection. Nature 424:1006–1007CrossRefGoogle Scholar
  34. HilleRisLambers J, Adler PB, Harpole WS, Levine JM, Mayfield MM (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248CrossRefGoogle Scholar
  35. Hoeferyz C (2003) For fundamentalism. Philos Sci 70:1401–1412CrossRefGoogle Scholar
  36. Holt RD (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proc Natl Acad Sci USA 106(Suppl. 2):19659–19665CrossRefGoogle Scholar
  37. Hubbell SP (1997) A unified theory of biogeography and relative species abundance and its application to tropical rain forests and coral reefs. Coral Reefs 16(Suppl.):S9–S21CrossRefGoogle Scholar
  38. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography monographs in population biology. Princeton University Press, PrincetonGoogle Scholar
  39. Hubbell SP, Foster RB (1986) Biology, chance and history and the structure of tropical rain forest tree communities. In: Diamond JM, Case TJ (eds) Community ecology. Harper and Row, New York, pp 314–329Google Scholar
  40. Hutchinson GE (1957) Concluding remarks, cold spring harbor symposium. Quant Biol 22:415–427CrossRefGoogle Scholar
  41. Jabot F, Chave J (2011) Analyzing tropical forest tree species abundance distributions using a non-neutral model and through approximate Bayesian inference. Am Nat 178:E37–E47CrossRefGoogle Scholar
  42. Jacquet C, Moritz C, Morissette L, Legagneux P, Massol F, Archambault P, Gravel D (2016) No complexity-stability relationship in empirical ecosystems. Nat Commun 7:12573CrossRefGoogle Scholar
  43. James A, Plank MJ, Rossberg AG, Beecham J, Emmerson M, Pitchford JW (2015) Constructing random matrices to represent real ecosystems. Am Nat 185:680–692CrossRefGoogle Scholar
  44. Janzen T, Haegeman B, Etienne RS (2015) A sampling formula for ecological communities with multiple dispersal syndromes. J Theor Biol 374:94–106CrossRefGoogle Scholar
  45. Jonzén N, Wilcox C, Possingham HP (2004) Habitat selection and population regulation in temporally fluctuating environments. Am Nat 164:103–114CrossRefGoogle Scholar
  46. Letten AD, Ke PJ, Fukami T (2017) Linking modern coexistence theory and contemporary niche theory. Ecol Monogr 87:161–177CrossRefGoogle Scholar
  47. Kadmon R, Allouche O (2007) Integrating the effects of area, isolation, and habitat heterogeneity on species diversity: a unification of island biogeography and niche theory. Am Nat 170:443–454CrossRefGoogle Scholar
  48. Kalyuzhny M, Seri E, Chocron R, Flather CH, Kadmon R, Shnerb NM (2014) Niche versus neutrality: a dynamical analysis. Am Nat 184:439–446CrossRefGoogle Scholar
  49. Kalyuzhny M, Kadmon R, Shnerb NM (2015) A neutral theory with environmental stochasticity explains static and dynamic properties of ecological communities. Ecol Lett 18:572–580CrossRefGoogle Scholar
  50. Knape J, de Valpine P (2012) Are patterns of density dependence in the global population dynamics database driven by uncertainty about population abundance? Ecol Lett 15:17–23CrossRefGoogle Scholar
  51. Kotler BP, Brown JS (1988) Environmental heterogeneity and the coexistence of desert rodents. Annu Rev Ecol Evol Syst 19:281–307CrossRefGoogle Scholar
  52. Krivan V, Cressman R, Schneider C (2008) The ideal free distribution: a review and synthesis of the game theoretic perspective. Theor Popul Biol 73:403–425CrossRefGoogle Scholar
  53. Lakatos I (1978) Falsification and the methodology of scientific research programmes. In: Lakatos I (ed) The methodology of scientific research programmes. Cambridge University Press, Cambridge, pp 8–101CrossRefGoogle Scholar
  54. Lakatos I, Zahar E (1978) Why did Copernicus’s research programme supersede Ptolemy’s? In: Lakatos I (ed) The methodology of scientific research programmes. Cambridge University Press, Cambridge, pp 8–101CrossRefGoogle Scholar
  55. Laplace PS (1902) A philosophical essay on probabilities, 6th edn. Dover Publications, New YorkGoogle Scholar
  56. Leigh EG Jr (2007) The neutral theory: a historical perspective. J Evol Biol 20:2075–2091CrossRefGoogle Scholar
  57. Levin SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur Award Lecture. Ecology 73:1943–1967CrossRefGoogle Scholar
  58. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–258CrossRefGoogle Scholar
  59. MacArthur R (1955) Fluctuations of animal populations and a measure of community stability. Ecology 36:533–536CrossRefGoogle Scholar
  60. MacArthur RH (1972) Geographical ecology. Princeton University Press, PrincetonGoogle Scholar
  61. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  62. Martín J, Lopez P (2005) Wall lizards modulate refuge use through continuous assessment of predation risk level. Ethology 111:207–219CrossRefGoogle Scholar
  63. Maruvka YE, Shnerb NM, Kessler DA, Ricklefs RE (2013) Model for macroevolutionary dynamics. Proc Natl Acad Sci USA 110:E2460–E2469CrossRefGoogle Scholar
  64. Matthews TJ, Whittaker RJ (2014) Neutral theory and the species abundance distribution: recent developments and prospects for unifying niche and neutral perspectives. Ecol Evol 4:2263–2277Google Scholar
  65. May RM (1972) Will a large complex system be stable? Nature 238:413–414CrossRefGoogle Scholar
  66. May RM (1974) Stability and complexity in model ecosystems. Princeton University Press, New JerseyGoogle Scholar
  67. May R (1999) Unanswered questions in ecology. Philos Trans R Soc Lond B Biol Sci 354:1951–1959CrossRefGoogle Scholar
  68. Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  69. Mayr E (1977) Darwin and natural selection: how Darwin may have discovered his highly unconventional theory. Am Sci 65:321–328Google Scholar
  70. McGill BJ, Maurer BA, Weiser MD (2006) Empirical evaluation of neutral theory. Ecology 87:1411–1423CrossRefGoogle Scholar
  71. Mitchell WA, Valone TJ (1990) The optimization research program: studying adaptations by their function. Q Rev Biol 65:43–52CrossRefGoogle Scholar
  72. Morris DW (1988) Habitat-dependent population regulation and community structure. Ecol Evol 2:253–269CrossRefGoogle Scholar
  73. Munoz F, Huneman P (2016) From the neutral theory to a comprehensive and multiscale theory of ecological equivalence. Q Rev Biol 91:321–342CrossRefGoogle Scholar
  74. Nicolson M, McIntosh RP, Nicholson M (2002) H.A. Gleason and the individualistic hypothesis revisited. Bull Ecol Soc Am 83:133–142Google Scholar
  75. Norris S (2003) Neutral theory: a new, unified model for ecology. BioScience 53:124–129CrossRefGoogle Scholar
  76. O’Dwyer JP, Chisholm R (2014) A mean field model for competition: from neutral ecology to the Red Queen. Ecol Lett 17:961–969CrossRefGoogle Scholar
  77. Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326CrossRefGoogle Scholar
  78. Pimm SL (1991) The balance of nature? Ecological issues in the conservation of species and communities. University of Chicago Press, ChicagoGoogle Scholar
  79. Rosenzweig ML (1981) A theory of habitat selection. Ecology 62:327–335CrossRefGoogle Scholar
  80. Rosindell J, Cornell SJ (2007) Species-area relationships from a spatially explicit neutral model in an infinite landscape. Ecol Lett 10:586–595CrossRefGoogle Scholar
  81. Rosindell J, Cornell SJ (2009) Species-area curves, neutral models, and long-distance dispersal. Ecology 90:1743–1750CrossRefGoogle Scholar
  82. Rosindell J, Hubbell SP, Etienne RS (2011) The unified neutral theory of biodiversity and biogeography at age ten. TREE 26:340–348Google Scholar
  83. Rosindell J, Hubbell SP, He F, Harmon LJ, Etienne RS (2012) The case for ecological neutral theory. TREE 27:203–208Google Scholar
  84. Russell B (1997) Religion and science, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  85. Simberloff D (1978) Using island biogeographic distributions to determine if colonization is stochastic. Am Nat 112:713–726CrossRefGoogle Scholar
  86. Slack NG (2010) G. Evelyn Hutchinson and the invention of modern ecology. Yale University Press, New HavenGoogle Scholar
  87. Storch D, Frynta D (1999) Evolution of habitat selection: stochastic acquisition of cognitive clues? Ecol Evol 13:591–600CrossRefGoogle Scholar
  88. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206CrossRefGoogle Scholar
  89. Vincent TL, Brown JS (2005) Evolutionary game theory, natural selection, and Darwinian dynamics. Cambridge University Press, New YorkCrossRefGoogle Scholar
  90. von Humboldt A (1849) Aspects of nature: in different lands and different climates, with scientific elucidations (trans: E. J. Sabine.). Longman, Brown, Green, and Longmans and J. Murray, LondonGoogle Scholar
  91. von Neumann J (1947) The works of the mind. In: Heywood RB (ed) The mathematician, vol 1. University of Chicago Press, Chicago, pp 1–9Google Scholar
  92. Welton NJ, McNamara JM, Houston AI (2003) Assessing predation risk: optimal behaviour and rules of thumb. Theor Popul Biol 64:417–430CrossRefGoogle Scholar
  93. Wennekes PL, Rosindell J, Etienne RS (2012) The neutral—niche debate: a philosophical perspective. Acta Biotheor 60:257–271CrossRefGoogle Scholar
  94. White GF (1789) The natural history of Selborne. Penguin, LondonGoogle Scholar
  95. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  96. Wilson WG, Osenberg CW, Schmitt RJ, Nisbet RM (1999) Complementary foraging behaviors allow coexistence of two consumers. Ecology 80:2358–2372CrossRefGoogle Scholar
  97. Wootton JT (2005) Field parameterization and experimental test of the neutral theory of biodiversity. Nature 433:309–312CrossRefGoogle Scholar
  98. Yodzis P (1981) The stability of real ecosystems. Nature 289:674–676CrossRefGoogle Scholar
  99. Ziebarth NL, Abbott KC, Ives AR (2010) Weak population regulation in ecological time series. Ecol Lett 13:21–31CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biological Sciences M/C 066University of Illinois at ChicagoChicagoUSA
  2. 2.Department of BiologyIndiana State UniversityTerre HauteUSA
  3. 3.Moffitt Cancer CenterTampaUSA

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