Abstract
Organic selection (the Baldwin Effect) by which an environmentally elicitedphenotypic adaptation comes under genotypic control following selectionwas proposed independently in 1896 by the psychologists James Baldwinand Conwy Lloyd Morgan and by the paleontologist Henry Fairfield Osborn.Modified forms of organic selection were proposed as autonomization bySchmalhausen in 1938, as genetic assimilation by Waddington in 1942, andas an explanation for evolution in changing environments or for speciationby Matsuda and West-Eberhard in the 1980s. Organic selection as amechanism mediating proximate environmental effects on the evolution ofmorphology and behaviour is the topic of this essay. Discussion includesthe context in which organic selection was proposed, Lamarckian or neo-Lamarckian implications of organic selection, Waddington’s experimentalstudies demonstrating the existence and efficacy of genetic assimilation,stabilizing selection and norms of reaction favoured by Schmalhausen, andMatsuda’s search for a mechanism of organic selection in endocrine changesand in heterochrony.
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References
Adams, M.B.: 1980, ‘Severtzov and Schmalhausen: Russian Morphology and the Evolutionary Synthesis’, in E. Mayr andW.B. Provine (eds.), The Evolutionary Synthesis: Perspectives on the Unification of Biology, Harvard University Press, Cambridge, MA, pp. 193–225.
Adams, M.B. (ed.): 1994, The Evolution of Theodosius Dobzhansky. Essays on His Life and Thought in Russia and America, Princeton University Press, Princeton.
Allen, G.E.: 1991, ‘Mechanistic and Dialectical Materialism in 20th Century Evolutionary Theory: The Work of Ivan I. Schmalhausen’, in L. Warren andH. Koprowski (eds.), New Perspectives on Evolution, Wiley-Liss, New York, pp. 15–36.
Amundson, R.: 1994, ‘John T. Gulick and the Active Organism. Adaptation, Isolation, and the Politics of Evolution’, in R. MacLeod andP.E. Rehbock (ed.), Darwin’s Laboratory: Evolutionary Theory and Natural History in the Pacific, University of Hawaii Press, Honolulu, pp. 110–139.
Arthur, W.: 1984, Mechanisms of Morphological Evolution: A Combined Genetic, Developmental and Ecological Approach, John Willey & Sons, Chichester.
Baldwin, J.M.: 1896, ‘A New Factor in Evolution’, The American Naturalist 30, 441–451, 536–553.
Baldwin, J.M.: 1902, Development and Evolution, Macmillan, New York.
Baldwin, J.M. (ed.): 1925, Dictionary of Philosophy and Psychology, New edition with corrections, 3 vols., Macmillan, New York.
Bateman, K.G.: 1959a, ‘The Genetic Assimilation of the Dumpy Phenotype’, Journal of Genetics 56, 341–351.
Bateman, K.G.: 1959b, ‘The Genetic Assimilation of Four Venation Phenocopies’, Journal of Genetics 56, 443–474.
Benjafield, J.G.: 1996, A History of Psychology, Allyn and Bacon, Boston.
Berven, K.A.: 1982, ‘The Genetic Basis of Altitudinal Variation in the Wood Frog, Rana sylvatica. 1. An Experimental Basis of Life History Traits’, Evolution 36, 962–983.
Boycott, A.E.: 1938, ‘Experiments on the Artificial Breeding of Limnaea involuta, Limnaea burnetti and Other Forms of Limnaea peregra’, Proceedings of the Malacological Society of London 23, 101–108.
Boycott, A.E.,Diver, C.,Garstang, S.L. andTurner, F.M.: 1930, ‘The Inheritance of Sincestrality in Limnaea peregra (Mollusca: Pulmonata)’, Philosophical Transactions of the Royal Society of London (B) 219, 51–131.
Bush, G.L.: 1969, ‘Sympatric Host Race Formation and Speciation in Frugivorous Flies of the Genus Rhagoletis (Diptera, Tephretidae)’, Evolution 23, 237–251.
Bush, G.L.: 1973, ‘The Mechanism of Sympatric Host Race Formation in the True Fruit Flies (Tephretidae)’, in M.J.D. White (ed.), Genetic Mechanisms of Speciation in Insects, Reidel Publishing Co., Dordrecht, pp. 3–23.
Cahan, E.: 1984, ‘The Genetic Psychologies of James Mark Baldwin and Jean Piaget’, Developmental Physiology 20, 128–135.
Capdevila, M.P. andGarcia-Bellido, A.: 1974, ‘Development and Genetic Analysis of bithorax Phenocopies in Drosophila’, Nature 250, 500–502.
Clarke, E.: 1974, ‘Morgan, Conwy Llyod’, Dictionary of Scientific Biography 9, 512–513.
Dennett, D.C., 1995, Darwin’s Dangerous Idea. Evolution and the Meanings of Life, Simon & Schuster, New York.
Dodson, S.: 1989a, ‘Predator-induced Reaction Norms: Cyclic Changes in Shape and Size can be Protective’, BioScience 39, 447–452.
Dodson, S.: 1989b, ‘The Ecological Role of Chemical Stimuli for the Zooplankton Predatorinduced Morphology in Daphnia’, Oecologia 78, 361–367 (Berlin).
Dun, R.B. andFraser, A.S.: 1959, ‘Selection for an Invariant Character, Vibrissa Number, in the House Mouse’, Australian Journal of Biological Science 21, 506–523.
Duncan, K.W.: 1985, ‘A Critique of the Concept of Genetic Assimilation as a Mechanism in the Evolution of the Terrestrial Talitrids (Amphipoda)’, Canadian Journal of Zoology 63, 2230–2232.
Frank, S.A.: 1996, ‘The Design of Natural and Artificial Adaptive Systems’, in M.S. Rose andG.V. Lauder (eds.), Adaptation, Academic Press, San Diego, pp. 451–505.
Fraser, A.S. andKindred, D.M.: 1960, ‘Selection for an Invariant Character, Vibrissa Number, in the House Mouse. II. Limits to Variability’, Australian Journal of Biological Science 13, 48–58.
French, R.M. andMessinger, A.: 1994, ‘Genes, Phenes and the Baldwin Effect: Learning and Evolution in a Simulated Population’, in R.A. Broks andP. Maes (eds.), Artificial Life IV, MIT Press, Cambridge, MA, pp. 277–282.
Gerhart, J. andKirschner, M.: 1997, Cells, Embryos, and Evoluton: Toward a Cellular and Developmental Understanding of Phenotypic Variation and Evolutionary Adaptability, Blackwell Science, Malden, MA.
Gibson, G. andHogness, D.S.: 1996, ‘Effect of Polymorphism in the Drosophila Regulatory Gene Ultrabithorax on Homeotic Stability’, Science 271, 200–203.
Gibson, G. andWagner, G.P.: 2000, ‘Canalization in Evolutionary Genetics: A Stabilizing Theory?’, BioEssays 22, 372–380.
Gilbert, J.J.: 1966, ‘Rotifer Ecology and Embryological Induction’, Science 151, 1234–1237.
Gilbert, J.J.: 1980, ‘Female Polymorphism and Sexual Reproduction in the Rotifer Asplanchna: Evolution of Their Relationships and Control by Dietary Tocopherol’, The American Naturalist 116, 409–431.
Gilbert, S.F.: 1994, ‘Dobzhansky, Waddington and Schmalhausen: Embryology and the Modern Synthesis’, in M.B. Adams (ed.), The Evoution of Theodosius Dobzhansky, Princeton University Press, Princeton, NJ, pp. 143–154.
Gilbert, S.F.: 2000, ‘Baldwin, Waddington, and Schmalhausen and the Foundation of Evolutionary Developmental Biology’, American Zoologist 40 (in press).
Gillespie, N.C.: 1990, ‘The Interface of Natural Theology and Science in the Ethology of W.H. Thorpe’, Journal of the History of Biology 23, 1–38.
Gottlieb, G.: 1987a, ‘Development of Species Identification in Ducklings: XIV. Malleability of Species-Specific Perception’, Journal of Comparative Psychology 101, 178–182.
Gottlieb, G.: 1987b, ‘The Developmental Basis of Evolutionary Change’, Journal of Comparative Psychology 101, 262–271.
Gottlieb, G.: 1992, Individual Development and Evolution: The Genesis of Novel Behaviour, Oxford University Press, New York.
Grant, V.: 1963, The Origin of Adaptations, Columbia University Press, New York.
Greene, E.: 1989, ‘A Diet-Induced Development Polymorphism in a Caterpillar’, Science 243, 643–646.
Hadorn, E.: 1961, Developmental Physiology and Lethal Factors, John Wiley & Sons, New York.
Hall, B.K.: 1984, ‘Developmental Processes Underlying Heterochrony as an Evolutionary Mechanism’, Canadian Journal of Zoology 62, 1–7.
Hall, B.K.: 1990, ‘Heterochronic Change in Vertebrate Development’, Seminars in Developmental Biology 1, 237–243.
Hall, B.K.: 1992, ‘Waddington’s Legacy in Development and Evolution’, American Zoologist 32, 113–122.
Hall, B.K.: 1998a, Evolutionary Developmental Biology, 2nd edn., Kluwer Academic Publishers, Dordrecht, The Netherlands.
Hall, B.K.: 1998b, ‘Epigenetics: Regulation not Replication’, Journal of Evolutionary Biology 11, 201–205.
Hall, B.K.: 1999, ‘The Paradoxical Platypus’, BioScience 49, 211–218.
Hall, B.K.: 2000, ‘Evolutionary Developmental Biology: Where Embryos and Fossils Meet’, in K.J. McNamara andN. Minugh-Purves (eds.), Human Evolution Through Developmental Change, Johns Hopkins University Press, Baltimore (in press).
Hall, B.K.andWake, M.H. (eds.): 1999, The Origin and Evolution of Larval Forms, Academic Press, San Diego.
Hardy, A.: 1965, The Living Stream: A Restatement of Evolution Theory and its Relation to the Spirit of Man, Collins, London.
Harvell, C.D.: 1990, ‘The Ecology and Evolution of Inducible Defenses’, Quarterly Review of Biology 65, 323–340.
Hinton, G.E. andNowlan, S.J.: 1987, ‘How Learning Can Guide Evolution’, Complex Syst. 1, 495–502. Technical Report CMU-CS-86–128, Carnegie Mellon University.
Ho, M-W.: 1984, ‘Environmental and Heredity in Development and Evolution’, in M.-W. Ho andP.J. Saunders (eds.), Beyond Neo-Darwinism: An Introduction to the New Evolutionary Paradigm, Academic Press, London, pp. 267–289.
Ho, M.-W.,Bolton, E. andSaunders, P.T.: 1983, ‘The Bithorax Phenocopy and Pattern Formation. 1. Spatiotemporal Characteristics of the Phenocopy Response’, Experimental Cell Biology 51, 282–290.
Hovasse, R.: 1950, Adaptation et Évolution, Hermann, Paris.
Huettel, M.D. andBush, G.L.: 1972, ‘The Genetics of Host Selection and its Bearing on Sympatric Speciation in Procecidochares (Diptera, Tephretidae)’, Entomology, Experimental and Applied 15, 465–480.
Huxley, J.S.: 1942, Evolution, The Modern Synthesis, Allen and Unwin, London.
Johnston, T.D. andGottlieb, G.: 1990, ‘Neophenogenesis: A Developmental Theory of Phenotypic Evolution’, Journal of Theoretical Biology 147, 471–495.
King, R.C. andStansfield, W.D.: 1985, A Dictionary of Genetics, 3rd edn., Oxford University Press, Oxford.
Lerner, I.M.: 1954, Genetic Homeostasis, Oliver and Boyd, Edinburgh.
Matsuda, R.: 179, ‘Abnormal Metamorphosis and Arthropod Evolution’, in Gupta, A.P. (ed.), Arthropod Phylogeny, Van Nostrand Reinhold Co., New York, pp. 137–256.
Matsuda, R.: 1982, ‘The Evolutionary Process in Talitrid Amphipods and Salamanders in Changing Environments, With a Discussion of “Genetic Assimilation” and Some Other Evolutionary Concepts’, Canadian Journal of Zoology 60, 733–749.
Matsuda, R.: 1987, Animal Evolution in Changing Enviornments with Special Reference to Abnormal Metamorphosis, John Wiley & Sons, New York.
Maynard Smith, J.: 1987, ‘When Learning Guides Evolution’, Nature 329, 761–762.
Maynard Smith, J.,Burian, R.,Kauffman, S.,Alberch, P.,Campbell, J.,Goodwin, B.,Lande, R.,Raup, D.andWolpert L.: 1985, ‘Developmental Constraints and Evolution’, Quarterly Review of Biology 60, 265–287.
Mayr, E.: 1973, Animal Species and Evolution, The Belknap Press of Harvard University Press, Cambridge, MA.
Mayr, E.: 1976, Evolution and Diversity of Life, The Belknap Press of Harvard University Press, Cambridge, MA.
McKinney, M.L. andMcNamara, K.J.: 1991, Heterochrony: The Evolution of Ontogeny, Plenum Press, New York/London.
Messerly, J.G.: 1996, Piaget’s Conception of Evolution: Beyond Darwin and Lamarck, Rowman & Littlefield Publishers, Inc., Lanham, MD.
Mikhailov, A.T.: 1997, ‘Epigenesis Versus Preformation: First Chapter of the Russian Embryological Research’, International Journal of Developmental Biology 41, 755–762.
Milner, R.: 1990, The Encyclopedia of Evolution. Humanity’s Search for Its Origin, Facts on File, New York.
Morgan, C.: 1896a, ‘Of Modification and Variation’, Science 4, 733–740.
Morgan, C.L.: 1896b, Habitat and Instinct, E. Arnold Press, London.
Morgan, C.L.: 1900, Animal Behaviour, E. Arnold Press, London.
Osborn, H.F.: 1896, ‘A Mode of Evolution Requiring Neither Natural Selection Nor the Inheritance of Acquired Characters’, Transactions of the New York Academy of Science 15, 141–142, 148.
Osborn, H.F.: 1897a, ‘Organic Selection’, Science 15, 583–587.
Osborn, H.F.: 1897b, ‘The Limits of Organic Selection’, The American Naturalist 31, 944–951.
Papaj, D.R.: 1994, ‘Optimizing Learning and its Effect on Evolutionary Change in Behaviour’, in L.A. Real (ed.), Behavioural Mechanisms in Evolutionary Ecology, The University of Chicago Press, Chicago, pp. 133–153.
Parsons, P.A.: 1981, ‘Habitat Selection and Speciation in Drosophila’, in W.R. Atchley andD. Woodra (eds.), Evolution and Speciation, Cambridge University Press, Cambridge, pp. 219–240.
Pearson, R.D.: 1985, ‘Duncan’s Critique of Matsuda’, Canadian Journal of Zoology 63, 2982–2983.
Pearson, R.D.: 1988, ‘Reviews’, Acta Biotheoretica 37, 31–32.
Piaget, J.: 1929a, ‘Les Races Lacustres de la Limnaea stagnalis L. Recherches sur les Rapports de l’Adaptation Hereditaires avec le Milieu’, Bulletin de Biologie, France et Belgique 63, 424–455.
Piaget, J.: 1929b, ‘L’adaptation de la Limnaea stagnalis au Milieu Lacustres de la Suisse Romande. Etude Biométrique et Génétique’, Revue Suisse Zoologie 36, 263–531.
Piaget, J.: 1966, ‘Observations sur le Mode d’Insertion et la Chute des Rameaux Secondaires Chez les Sedum’, Candollea 21–22, 137–239.
Piaget, J.: 1978, Behaviour and Evolution, Pantheon Books, New York.
Piaget, J.: 1980, Adaptation and Intelligence: Organic Selection and Phenocopy, University of Chicago Press, Chicago [Translation of Adaptation Vitale et Psychologie de l’Intelligence: Sélection Organique et Phénocopie, 1974, Hermann, Paris].
Piatelli-Palmerini, M. (ed.): 1980, Language and Learning: The Debate Between Jean Piaget and Noam Chomsky, Routledge & Kegan Paul, London.
Polikoff, D.: 1981, ‘C. H. Waddington and Modern Evolutionary Theory’, Evolutionary Theory 5, 143–168.
Provine, W.B.: 1986, Sewall Wright and Evolutionary Biology, The University of Chicago Press, Chicago.
Rainger, R.: 1991, An Agenda for Antiquity: Henry Fairfield Osborn and Vertebrate Paleontology at the American Museum of Natural History, 1890–1935, The University of Alabama Press, Tuscaloosa/London.
Rendel, J.M.: 1968, ‘Genetic Control of Developmental Processes’, in Lewontin, R.C. (ed.), Population Biology and Evolution, Syracuse University Press, Syracuse, NY, pp. 47–68.
Richards, R.J.: 1987, Darwin and the Emergence of Evolutionary Theories of Mind and Behavior, Chicago University Press, Chicago.
Robertson, A.: 1977, ‘Conrad Hal Waddington,’, Biographical Memoirs of Fellows of the Royal Society 23, 575–622.
Rollo, C.D.: 1995, Phenotypes: Their Epigenetics, Ecology and Evolution, Chapman & Hall, London.
Russell, J.: 1978, The Acquisition of Knowledge, Macmillan, London.
Sarkar, S.: 1999, ‘From the Reaktionsnorm to the Adaptive Norm: The Norm of Reaction, 1909–1960’, Biology and Philosophy 14, 235–252.
Scharloo, W.: 1991, ‘Canalization: Genetic and Developmental Aspects’, Annual Reviews in Ecology and Systematics 22, 65–93.
Schmalhausen, I.I.: 1938, The Integrating Factors of Evolution, Nature (Priroda), Leningrad.
Schmallhausen, I.I.: 1942, The Organism as a Whole in Development and Evoluton, 2nd edn., Moscow.
Schmalhausen, I.I.: 1949, Factors of Evolution. The Theory of Stabilizing Selection, translated by I. Dordick andT. Dobzhansky (eds.), Blakiston, Philadelphia, PA. (Reprinted with a new foreword by David B. Wake, University of Chicago Press, Chicago, 1986.)
Schwenk, K.: 1994/ 95, ‘A Utilitarian Approach to Evolutionary Constraint’, Zoology 98, 251–262.
Shine, R. andGuillette, L.J. Jr.: 1988, ‘The Evolution of Viviparity in Reptiles: A Physiological Model and its Ecological Consequences’, Journal of Theoretical Biology 132, 43–50.
Simpson, G.G.: 1953, ‘The Baldwin Effect’, Evolution 7, 110–117.
Sinha, C.: 1984, ‘A Socio-Naturalistic Approach to Human Development’, in M.-W. Ho andP.J. Saunders (eds.), Beyond Neo-Darwinism, in Introduction to the new Evolutionary Paradigm, Academic Press, London, pp. 331–362.
Stearns, S.C.: 1989, ‘The Evolutionary Significance of Phenotypic Plasticity’, BioScience 37, 436–445.
Stearns, S.C.: 1992, The Evolution of Life Histories, Oxford University Press, Oxford.
Stern, C.: 1958, ‘Selection for Subthreshold Differences and the Origin of Pseudoexogenous Adaptations’, The American Naturalist 92, 313–316.
Sterm, C.: 1959, ‘Variation and Heredity Transmission’, Proceedings of the American Philosophical Society 103, 183–189.
Stern, C.D.: 2000, ‘Conrad H. Waddington’s Contribution to Avian and Mammalian Development, 1930–1940’, International Journal of Developmental Biology 44, 15–22.
Thom, R.: 1989, ‘An Inventory ofWaddingtonian Concepts’, in B.C. Goodwin andP. Saunders (eds.), Theoretical Biology, Epigenetic and Evolutionary Order from Complex Systems, Edinburgh University Press, Edinburgh, pp. 1–7.
Thompson, J.N. andThoday, J.M.: 1975, ‘Genetic Assimilation of Part of a Mutant Phenotype’, Genetical Research 6, 149–162.
Thomson, K.S.: 1988, Morphogenesis and Evolution, Oxford University Press, Oxford.
Thorpe, W.H.: 1930, ‘Biological Races in Insects and Allied Groups’, Biological Reviews of the Cambridge Philosophical Society 5, 177–212.
Thorpe, W.H.: 1940, ‘Ecology and the Future of Systematics’, in J. Huxley (ed.), The New Systematics, Oxford University Press, Oxford, pp. 341–364.
Thorpe, W.H.: 1945, ‘The Evolutionary Significance of Habitat Selection’, J. Animal Ecology 14, 67–70.
Van der Weele, C.: 1999, Images of Development. Environmental Causes in Ontogeny, SUNY Press, Albany, NY.
Vonèche, J.: 1982, ‘Evolution, Development and the Growth of Knowledge’, in J. Broughton andD. Freeman-Noir (eds.), The Cognitive-Developmental Psychology of James Mark Baldwin, Ablex, Norwood, NJ, pp. 51–79.
Vorobyeva, E.I.: 1987, ‘I. I. Schmalhausen’s Conception of Onthogenesis Evolution’, in V.P. Delfino (ed.), International Symposium on Biological Evolution, Adriatica Editrice, Bari, pp. 369–381.
Vorobyeva, E.I.: 1989, ‘I. I. The Evolutionary Principle of Dynamic Stability’, Rivista di Biologia-Biology Forum 82, 313–315.
Waddington, C.H.: 1940, Organisers and Genes, Cambridge University Press, Cambridge.
Waddington, C.H.: 1942, ‘Canalization of Development and the Inheritance of Acquired Characters’, Nature 150, 563.
Waddington, C.H.: 1953a, ‘Genetic Assimilation of an Acquired Character’, Evolution 7, 118–126.
Waddington, C.H.: 1953b, ‘The “Baldwin Effect,” “Genetic Assimilation” and “Homeostasis”’, Evolution 7, 386–387.
Waddington, C.H.: 1956a, ‘Genetic Assimilation of the Bithorax Phenotype’, Evolution 10, 1–13.
Waddington, C.H.: 1956b, ‘The Genetic Basis of the ‘Assisimlated Bithorax Stock’, Journal of Genetics 55, 240–245.
Waddington, C.H.: 1958, ‘Inheritance of Acquired Characters’, Proceedings of the Linnean Society of London 169, 41–62.
Waddington, C.H.: 1959, ‘Canalisation of Development and Genetic Assimilation of Acquired Characters’, Nature 183, 1654–1655.
Waddington, C.H.: 1961, ‘Genetic Assimilation’, Advances in Genetics 10, 257–293.
Waddington, C.H.: 1975, The Evolution of an Evolutionist, Cornell University Press, Ithaca/New York.
Wagner, G.P. andAltenberg, L.: 1996, ‘Complex Adaptations and the Evolution of Evolvability’, Evolution 50, 967–976.
Wagner, G.P.,Booth, G. andBagheri-Chaichian, H.: 1997, ‘A Population Genetic Theory of Canalization’, Evolution 51, 329–347.
Wagner, G.P. andSchwenk, K.: 2000, ‘Evolutionary Stable Configurations: Functional Integration and the Evolution of Phenotypic Stability’, Evolutionary Biology 31, 155–217.
Wake, D.B.: 1986, ‘Foreword’, in Factors of Evolution. The Theory of Stabilizing Selection by I. I. Schmalhausen, University of Chicago Press, Chicago, pp. x-vii.
Wake, D.B.: 1996, ‘Schmalhausen’s Evolutionary Morphology and its Value in Formulating Research Strategies’, Memorie della Società Italiano di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 28, 129–132.
West-Eberhard, M.J.: 1986, ‘Alternative Adaptations, Speciation, and Phylogeny (a Review)’, Proceedings of the National Academy of Science USA 83, 1388–1392.
West-Eberhard, M.J.: 1989, ‘Phenotypic Plasticity and the Origins of Diversity’, Annual Reviews in Ecology and Systematics 20, 249–278.
Wilkins, A.S.: 1997, ‘Canalization: A Molecular Genetic Perspective’, BioEssays 19, 257–262.
Wright, S.: 1968, Evolution and the Genetics of Populations, Volume 1, The University of Chicago Press, Chicago, IL.
Yoxen, E.: 1986, ‘Form and Strategy in Biology: Reflections on the Career of C. H. Waddington’, in T.J. Horder,J.A. Witkowski andC.C. Wylie (eds.), A History of Embryology, Cambridge University Press, Cambridge, pp. 309–329.
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Hall, B.K. Organic Selection: Proximate Environmental Effects on the Evolution of Morphology and Behaviour. Biology & Philosophy 16, 215–237 (2001). https://doi.org/10.1023/A:1006773408919
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DOI: https://doi.org/10.1023/A:1006773408919