Abstract
In a previous study, using experimental metapopulations of the flour beetle, Tribolium castaneum, we investigated phase III of Wright's shifting balance process (Wade and Griesemer 1998). We experimentally modeled migration of varying amounts from demes of high mean fitness into demes of lower mean fitness (as in Wright's characterization of phase III) as well as the reciprocal (the opposite of phase III). We estimated the “meta-populational heritability” for this level of selection by regression of offspring deme means on the weighted parental deme means.
Here we develop a Punnett Square representation of the inheritance of the group mean to place our empirical findings in a conceptual context similar to Mendelian inheritance of individual traits. The comparison of Punnett Squares for individual and group inheritance shows how the latter concept can be rigorously defined and extended despite the lack of explicitly formulated, simple “Mendelian” laws of inheritance at the group level. Whereas Wright's phase III combines both interdemic selection and meta-populational inheritance, our formulation separates the issue of meta-populational heritability from that of interdemic selection. We use this conceptual context to discuss the controversies over the levels of selection and the units of inheritance.
Similar content being viewed by others
References
Arnold, S.J. and Wade, M.J.: 1984, ‘On the Measurement of Selection in Natural and Laboratory Populations: Theory’, Evolution 38, 709–719.
Boyd, R. and Richerson, P.J.: 1985, Culture and the Evolutionary Process, University of Chicago Press, Chicago, IL.
Brandon, R.: 1990, Adaptation and Environment, Princeton University Press, Princeton, NJ.
Crow, J.F.: 1962, ‘Population Genetics: Selection’, in W.J. Burdett (ed.), Methodology in Human Genetics, Holden-Day, San Francisco, pp. 53–75.
Crow, J.F., Engels, W.R. and Denniston, C.: 1990, ‘Phase Three of Wright's Shifting-Balance Theory’, Evolution 44, 233–247.
Dawkins, R.: 1976, The Selfish Gene, Oxford University Press, Oxford.
Dawkins, R.: 1982, The Extended Phenotype, Oxford University Press, Oxford.
Falconer, D.S.: 1987, Introduction to Quantitative Genetics, Third Edition, Longman, NY.
Fisher, R.A.: 1958, The Genetical Theory of Natural Selection, Clarendon Press, Oxford.
Frank, S.: 1995, ‘George Price's Contributions to Evolutionary Genetics’, Journal of Theoretical Biology 175, 373–388.
Goodnight, C.J.: 1988, ‘Population Differentiation and the Transmission of Density Effects between Generations’, Evolution 42, 399–403.
Goodnight, C.J.: 1989, ‘Population Differentiation and the Correlation among Traits at the Population Level’, American Naturalist 133, 888–900.
Goodnight, C.J., Schwartz, J.M. and Stevens, L.: 1992, ‘Contextual Analysis of Models of Group Selection, Soft Selection, Hard Selection, and the Evolution of Altruism’, American Naturalist 140, 743–761.
Griesemer, J.: 1998a, ‘Commentary: The Case for Epigenetic Inheritance in Evolution’, Journal of Evolutionary Biology 11(2), 193–200.
Griesemer, J.: 1998b, ‘Materials for the Study of Evolutionary Transition (review of Maynard Smith and Szathmáry 1995, The Major Transitions in Evolution)’, Biology and Philosophy, in press.
Griffing, B.: 1977, ‘Selection for Populations of Interacting Genotypes’, in E. Pollack, O. Kempthorne and T.B. Bailey Jr. (eds.), Proceedings of the International Conference on Quantitative Genetics, Iowa State University Press, Ames, pp. 413–434.
Heisler, L. and Damuth, J.D.: 1987, ‘A Method for Analysing Selection in Hierarchically Structured Populations’, American Naturalist 130, 582–602.
Hull, D.: 1980, ‘Individuality and Selection’, Annual Reviews of Ecology and Systematics 11, 311–332.
Hull, D.: 1981, ‘The Units of Evolution: A Metaphysical Essay’, in U. Jensen and R. Harré (eds.), The Philosophy of Evolution, The Harvester Press, Brighton, pp. 23–44.
Hull, D.: 1988, Science as a Process, University of Chicago Press, Chicago, IL.
Kelly, J.K.: 1994, ‘The Effect of Scale Dependent Processes on Kin Selection: Mating and Density Regulation’, Theoretical Population Biology 46, 32–57.
Lande, R. and Arnold, S.J.: 1983, ‘The Measurement of Selection on Correlated Characters’, Evolution 36, 1210–1226.
Lewontin, R.C.: 1970, ‘The Units of Selection’, Annual Review of Ecology and Systematics 1, 1–18.
Lloyd, E.: 1988, The Structure and Confirmation of Evolutionary Theory, Greenwood Press, NY.
Michod, R.: 1982, ‘The Theory of Kin Selection’, Annual Review of Ecology and Systematics 13, 23–55.
Moore, F.B.-G. and Tonsor, S.J.: 1994, ‘A Simulation of Wright's Shifting-Balance Process: Migration and the Three Phases’, Evolution 48, 69–80.
Price, G.R.: 1970, ‘Selection and Covariance’, Nature 227, 520–522.
Price, G.R.: 1972, ‘Extension of Covariance Mathematics’, Annals of Human Genetics 35, 485–490.
Sarkar, S.: 1994, ‘The Selection of Alleles and the Additivity of Variance’, in D. Hull, M. Forbes and R.M. Burian (eds.), PSA 1994, Vol. 2, Philosophy of Science Association, East Lansing, MI, pp. 3–12.
Slatkin, M.: 1981, ‘Populational Heritability’, Evolution 35, 859–871.
Sober, E.: 1984, The Nature of Selection, MIT Press, Cambridge, MA.
Tanaka, Y.: 1996, ‘A Quantitative Genetic Model of Group Selection’, American Naturalist 148, 660–683.
Vrba, E.S.: 1980, ‘Evolution, Species and Fossils: How Does Life Evolve?’, South African Journal of Science 76, 61–84.
Wade, M.J.: 1978, ‘A Critical Review of the Models of Group Selection’, Quarterly Review of Biology 53, 101–114.
Wade, M.J.: 1979, ‘Sexual Selection and Variance in Reproductive Success’, American Naturalist 114, 742–747.
Wade, M.J.: 1980, ‘Kin Selection: Its Components’, Science 210, 665–667.
Wade, M.J.: 1982, ‘Group Selection: Migration and the Differentiation of Small Populations’, Evolution 36, 949–961.
Wade, M.J.: 1985, ‘Hard Selection, Soft Selection, Kin Selection, and Group Selection’, American Naturalist 125, 61–73.
Wade, M.J. and Breden, F.J.: 1981, ‘Effect of Inbreeding on the Evolution of Altruistic Behaviors by Kin Selection’, Evolution 35, 844–858.
Wade, M.J. and Breden, F.J.: 1987, ‘Kin Selection in Complex Groups: Mating Structure, Migration Structure and the Evolution of Social Behaviors’, in B.D. Chepko-Sade and Z.T. Halperin (eds.),Mammalian Dispersal Patterns, University of Chicago Press, Chicago, IL, pp. 273–283.
Wade, M.J. and Griesemer, J.R.: 1998, ‘Populational Heritability: Empirical Studies of Evolution in Metapopulations’, American Naturalist 151(3), 135–147.
Wade, M.J. and Goodnight, C.J.: 1991, ‘Wright's Shifting Balance Theory: an Experimental Study’, Science 253, 1015–1018.
Wade, M.J. and Kalisz, S.: 1990, ‘The Causes of Natural Selection’, Evolution 44, 1947–1955.
Wade, M.J. and McCauley, D.E.: 1980, ‘Group Selection: the Phenotypic and Genotypic Differentiation of Small Populations’, Evolution 34, 799–812.
Wade, M.J. and McCauley, D.E.: 1984, ‘Group Selection: The Interaction of Local Deme Size and Migration in the Differentiation of Small Populations’, Evolution 38, 1047–1058.
Williams, G.C.: 1966, Adaptation and Natural Selection, Princeton University Press, Princeton.
Wimsatt, W.: 1980, ‘Reductionistic Research Strategies and their Biases in the Units of Selection Controversy’, in T. Nickles (ed.), Scientific Discovery, Vol. II: Historical and Scientific Case Studies, D. Reidel, Dordrecht, pp. 213–259.
Wimsatt, W.: 1981, ‘Units of Selection and the Structure of the Multi-Level Genome’, in P. Asquith and R. Giere (eds.), PSA 1980, Vol. 2, Philosophy of Science Association, East Lansing, MI, pp. 122–183.
Wimsatt, W.: 1995, The Analytic Geometry of Genetics: the Evolution of Punnett Squares, ms., 31 pp.
Wright, S.: 1931, ‘Evolution in Mendelian Populations’, Genetics 16, 97–159.
Wright, S.: 1959, ‘Physiological Genetics, Ecology of Populations, and Natural Selection’, Perspectives in Biology and Medicine 3, 107–151.
Wright, S.: 1978, Evolution and the Genetics of Populations, Vol. 4, University of Chicago Press, Chicago, IL.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Griesemer, J.R., Wade, M.J. Populational Heritability: Extending Punnett Square Concepts to Evolution at the Metapopulation Level. Biology & Philosophy 15, 1–17 (2000). https://doi.org/10.1023/A:1006501313374
Issue Date:
DOI: https://doi.org/10.1023/A:1006501313374