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The Empirical Nonequivalence of Genic and Genotypic Models of Selection: A (Decisive) Refutation of Genic Selectionism and Pluralistic Genic Selectionism

Published online by Cambridge University Press:  01 January 2022

Robert N. Brandon  and
H. Frederik Nijhout
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Abstract

Genic selectionists (Williams 1966; Dawkins 1976) defend the view that genes are the (unique) units of selection and that all evolutionary events can be adequately represented at the genic level. Pluralistic genic selectionists (Sterelny and Kitcher 1988; Waters 1991; Dawkins 1982) defend the weaker view that in many cases there are multiple equally adequate accounts of evolutionary events, but that always among the set of equally adequate representations will be one at the genic level. We describe a range of cases all involving stable equilibria actively maintained by selection. In these cases genotypic models correctly show that selection is active at the equilibrium point. In contrast, the genic models have selection disappearing at equilibrium. For deterministic models this difference makes no difference. However, once drift is added in, the two sets of models diverge in their predicted evolutionary trajectories. Thus, contrary to received wisdom on this matter, the two sets of models are not empirically equivalent. Moreover, the genic models get the facts wrong.

Type
Research Article
Information
Philosophy of Science , Volume 73 , Issue 3 , July 2006 , pp. 277 - 297
Copyright
Copyright © The Philosophy of Science Association

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Footnotes

‡

The authors wish to thank Mark Rausher, Alex Rosenberg, Ken Waters, and the Duke Philosophy of Biology Discussion Group for comments on earlier drafts. We also thank two anonymous reviewers for this journal who offered helpful criticisms.

References

Antonovics, J., Ellstrand, N. C., and Brandon, R. N. (1988), “Genetic Variation and Environmental Variation: Expectations and Experiments,” in Gottlieb, L. D. and Jain, S. K. (eds.), Plant Evolutionary Biology. London: Chapman and Hall, 275–303.CrossRefGoogle Scholar
Bamshad, M., and Wooding, S. P. (2003), “Signatures of Natural Selection in the Human Genome,” National Review of Genetics 4:99–111.CrossRefGoogle ScholarPubMed
Barton, N. H., and Turelli, M. (1989), “Evolutionary Quantitative Genetics: How Little Do We Know?” Annual Review of Genetics 23:337–370.CrossRefGoogle ScholarPubMed
Brandon, R. N. (1982), “The Levels of Selection,” in Asquith, P. and Nickles, T. (eds.), PSA 1982: Proceedings of the 1982 Biennial Meeting of the Philosophy of Science Association, Vol. 1. East Lansing, MI: Philosophy of Science Association, 315–323.Google Scholar
Brandon, R. N. (1990), Adaptation and Environment. Princeton, NJ: Princeton University Press.Google Scholar
Brandon, R. N. (2001), “Organism and Environment Revisited,” in Singh, R., Paul, D., Krimbas, C., and Beatty, J. (eds.), Thinking about Evolution: Historical, Philosophical, and Political Perspectives. Cambridge: Cambridge University Press, 336–352.Google Scholar
Brandon, R. N. (2005), “The Difference between Selection and Drift: A Reply to Millstein,” Biology and Philosophy 20:153–170.CrossRefGoogle Scholar
Brandon, R. N. (2006), “The Principle of Drift: Biology's First Law,” Journal of Philosophy 103(7): 319–335.CrossRefGoogle Scholar
Brandon, R. N., and Antonovics, J. (1996), “The Coevolution of Organism and Environment,” in Brandon, R., Concepts and Methods in Evolutionary Biology. Cambridge: Cambridge University Press.Google Scholar
Brandon, R. N., and Burian, R., eds. (1984), Genes, Organisms, Populations: Controversies over the Units of Selection. Cambridge, MA: MIT Press, Bradford Books.Google Scholar
Dawkins, R. (1976), The Selfish Gene. Oxford: Oxford University Press.Google Scholar
Dawkins, R. (1982), The Extended Phenotype. Oxford: Freeman.Google Scholar
Edwards, A. W. F. (1992), Likelihood. Baltimore: Johns Hopkins Press.Google Scholar
Endler, J. A. (1986), Natural Selection in the Wild. Princeton, NJ: Princeton University Press.Google Scholar
Fisher, R. A. (1930), The Genetical Theory of Natural Selection. Oxford: Clarendon.CrossRefGoogle Scholar
Godfrey-Smith, P., and Lewontin, R. C. (1993), “The Dimensions of Selection,” Philosophy of Science 60:373–395.Google Scholar
Gould, Stephen J. (2002), The Structure of Evolutionary Theory. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Kerr, B., and Godfrey-Smith, P. (2002), “Individualist and Multi-level Perspectives on Selection in Structured Populations,” Biology and Philosophy 17:477–517.CrossRefGoogle Scholar
Kingsolver, J. G., et al. (2001), “The Strength of Phenotypic Selection in Natural Populations,” American Naturalist 157(3): 245–261.CrossRefGoogle ScholarPubMed
Kreitman, M. (2000), “Methods to Detect Selection in Populations with Applications to the Human,” Annual Review of Genomics and Human Genetics 1:539–559.CrossRefGoogle ScholarPubMed
Laland, K. N., Odling-Smee, F. J., and Feldman, M. W. (1996), “The Evolutionary Consequences of Niche Construction: A Theoretical Investigation Using Two-Locus Theory,” Journal of Evolutionary Biology 9:293–316.CrossRefGoogle Scholar
Lewontin, R. C. (1983), “Gene, Organism and Environment,” in Bendall, D. S. (ed.), Evolution from Molecules to Men. Cambridge: Cambridge University Press, 273–285.Google Scholar
Lloyd, E. A. (1988), The Structure and Confirmation of Evolutionary Theory. New York: Greenwood.Google Scholar
Lloyd, E. A. (2001), “Different Questions: Levels and Units of Selection,” in Singh, Rama S., Krimbas, Costas B., Paul, Diane B., and Beatty, John (eds.), Thinking about Evolution: Historical, Philosophical, and Political Perspectives. New York: Cambridge University Press, 267–291.Google Scholar
Lloyd, E. A. (2005), “Why the Gene Will Not Return,” Philosophy of Science 72:287–310.CrossRefGoogle Scholar
Matthen, M., and Ariew, A. (2002), “Two Ways of Thinking about Fitness and Natural Selection,” Journal of Philosophy 99:55–83.CrossRefGoogle Scholar
Nijhout, H. F. (2003), “The Nature of Robustness in Development,” BioEssays 24:553–563.CrossRefGoogle Scholar
Nijhout, H. F. (forthcoming), “Complex Traits: Genetics and Evolution.”Google Scholar
Rice, S. H. (1998), “The Evolution of Canalization and the Breaking of Von Baer’s Laws: Modeling the Evolution of Development with Epistasis,” Evolution 52:647–645.CrossRefGoogle ScholarPubMed
Rice, S. H. (2004), Evolutionary Theory. Sunderland, MA: Sinauer Associates.Google Scholar
Roughgarden, J. (1979), Theory of Population Genetics and Evolutionary Ecology: An Introduction. New York: Macmillan.Google Scholar
Sober, E. (1984), The Nature of Selection. Cambridge, MA: MIT Press.Google Scholar
Sober, E., and Lewontin, R. C. (1982), “Artifact, Cause and Genic Selection,” Philosophy of Science 49:157–180.CrossRefGoogle Scholar
Sober, Elliot, and Wilson, David Sloan (1998), Unto Others. Cambridge, MA: Harvard University Press.Google Scholar
Sterelny, K., and Kitcher, P. (1988), “The Return of the Gene,” Journal of Philosophy 85(7): 339–361.CrossRefGoogle Scholar
Turelli, M., and Barton, N. H. (1990), “Dynamics of Polygenic Characters under Selection,” Theoretical Population Biology 38:1–57.CrossRefGoogle Scholar
Van der Steen, W. J., and Van den Berg, H. A. (1999), “Dissolving Disputes over Genic Selectionism,” Journal of Evolutionary Biology 12:184–187.CrossRefGoogle Scholar
Walsh, D., Lewens, T., and Ariew, A. (2002), “Trials of Life: Natural Selection and Random Drift,” Philosophy of Science 69:452–473.CrossRefGoogle Scholar
Waters, K. (1991), “Tempered Realism about the Force of Selection,” Philosophy of Science 58:553–573.CrossRefGoogle Scholar
Waters, K. (2005), “Why Genic and Multilevel Selection Theories Are Here to Stay,” Philosophy of Science 72:311–333.CrossRefGoogle Scholar
Wilson, R. A. (2003), “Pluralism, Entwinement, and the Levels of Selection,” Philosophy of Science 70:531–552.CrossRefGoogle Scholar
Williams, G. C. (1966), Adaptation and Natural Selection. Princeton, NJ: Princeton University Press.Google Scholar
Wimsatt, W. C. (1980), “Reductionistic Research Strategies and Their Biases in the Units of Selection Controversy,” in T. Nickles (ed.), Scientific Discovery, Vol. 2, Historical and Scientific Case Studies. Dordrecht: Reidel, 213–259.CrossRefGoogle Scholar
Yang, Z., and Bielawski, J. P. (2000), “Statistical Methods for Detecting Molecular Adaptation,” Trends in Ecology and Evolution 15:496–503.CrossRefGoogle ScholarPubMed