Abstract
Homology continues to be a concept of central importance in the study of phylogenetic relations, but its relation to ontogenetic processes remains problematical. A definition of homology in terms of equivalent morphogenetic processes is defined and applied to the comparative study of tetrapod limbs. This allows for a consistent treatment of relations of similarity and difference of appendage structure in vertebrates, and the distinction between fishes fins and tetrapod limbs in terms of the concept of equivalence is described. The role of genes can also be clarified in this context, in particular the influence of the Hox 4 complex in determining digit character and the homeotic transformations that arise from changes in their expression patterns. It is argued that these observations are not compatible with the notion of homology between individual digits (I, II, III, etc.) across the tetrapods, and that homology cannot be consistently identified with gene action. The relations between homology and the properties of the morphogenetic limb field are discussed.
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References
Baleuns, A., M.T. Gasseling and J.W. Saunders (1970). Spatio-temporal distribution of a zone that controls anteroposterior polarity in the limb bud of the chick and other bird embryos. Amer. Zool. 10: 323.
Bateson, W. (1894). Materials for the Study of Variation. Cambridge Univ. Press. Reprint (1992). Johns Hopkins Univ. Press.
Beer, Sir Gavin de (1971). Homology: an Unsolved Problem. Oxford Univ. Press.
Ben-Ze'ev, A., S.R. Farmer and S. Penman (1980). Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchorage-dependent fibroblasts. Cell 21: 365–372.
Ben-Ze'ev, A., G.S. Robinson, N.L.R. Bucher and S.R. Farmer (1988). Cell-cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes. Proc. Nat. Acad. Sci. USA 85: 2161–2165.
Cassirer, E. (1950). The Problem of Knowledge. New Haven, Yale Univ. Press.
Coates, M.I. and J.A. Clack (1990). Polydactyly in the earliest known tetrapod limbs. Nature 347: 66–69.
Fallon, J.F. and G.M. Crosby (1977). Polarizing zone activity in limb bud amniotes. In: D.A. Ede, J.R. Hinchliffe and M. Balls, eds., Vertebrate Limb and Somite Morphogenesis, pp. 55–69. Cambridge Univ. Press.
Goethe, J.W. (1830). Principes de Philosophie zoologiques discutes en Mars, 1830, au sein de l'Academie Royale des Sciences. Naturwiss. Schriften, Werke VII, 189.
Goodwin, B.C. (1982). Development and evolution. J. theoret. Biol. 97: 43–55.
Goodwin, B.C. (1989). Evolution and the generative order. In: B.C. Goodwin and P.T. Saunders, eds., Theoretical Biology: Epigenetic and Evolutionary Order from Complex Systems, pp. 89–100. Edinburgh Univ. Press.
Goodwin, B.C. (1993). Development as a robust natural process. In: W.D. Stein and F. Varela, eds., Thinking About Biology. Santa Fe Institute Studies in the Sciences of Complexity. Addison-Wesley.
Goodwin, B.C. and L.E.H. Trainor (1983). The ontogeny and phylogeny of the pentadactyl limb. In: B.C. Goodwin, N.J. Holder and C.C. Wylie, eds., Development and Evolution, pp. 75–98. Cambridge Univ. Press.
Goodwin, B.C., S.A. Kauffman and J.D. Murray (1993). Is morphogenesis an intrinsically robust process? J. theoret. Biol. 163: 135–144.
Hall, B.K. (1991). Evolutionary Developmental Biology. Chapman and Hall.
Harrison, R.G. (1921). On relations of symmetry in transplanted limbs. J. exp. Zool. 32: 1–136.
Hinchliffe, J.R. (1990). Towards a homology of process: evolutionary implications of experimental studies on the generation of skeletal pattern in avian limb development. In: J. Maynard Smith and G. Vida, eds., Organizational Constraints on the Dynamics of Evolution, pp. 119–131. Manchester Univ. Press.
Hinchliffe, J.R. and M. Hecht (1984). Homology of the bird wing skeleton: embryological versus palaeontological evidence. Evolutionary Biology 30: 21–39.
Ho, M.W. (1990). An exercise in rational taxonomy. J. theoret. Biol. 169: 43–57.
Jarvik, E. (1980). Basic Structure and Evolution of Vertebrates, Vol. 2. London, Academic Press.
Maden, M. (1982). Vitamin A and pattern formation in the regenerating limb. Nature 295: 672–675.
Mehta, P., J.S. Bertram and W.R. Loewenstein (1989). The actions of retinoids on cellular growth correlate with their actions on gap junctional communication. J. Cell Biol. 108: 1053–1065.
Morgan, B.A., J.C. Izpisua-Belmonte, D. Duboule and C.J. Tabin (1992). Ectopic expression of Hox-4.6 in the avian limb bud causes homeotic transformation of anterior structures. Nature.
Newman, S.A. and W.D. Comper (1990). ‘Generic’ physical mechanisms of morphogenesis and pattern formation. Development 110: 1–18.
Oster, G.F. and P. Alberch (1982). Evolution and bifurcation of developmental programs. Evolution 36: 444–459.
Oster, G.F., J.D. Murray and A. Harris (1983). Mechanical aspects of mesenchymal morphogenesis. J. Embryol. exp. Morph. 78: 83–125.
Oster, G.F., J.D. Murray and P. Maini (1985). A model for chondrogenic condensations in the developing limb: the role of extracellular matrix and cell tractions. J. Embryol. exp. Morphol. 89: 93–112.
Oster, G.F., N. Shubin, J.D. Murray and P. Alberch (1988). Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 42: 862–884.
Pautou, M.-P. (1973) Analyse de la morphogenèse du pied des Oiseaux à l'aide de melanges cellulaires interspécifiques. J. embryol. exp. Morphol. 69: 1–6.
Shubin, N.H. and P. Alberch (1986). A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evol. Biol. 20: 319–387.
Tabin, C.J. (1992). Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development 116: 289–296.
Tickle, C., L. Alberts, L. Wolpert and J. Lee (1982). Local application of retinoic acid to the limb bud mimics the action of the polarizing zone. Nature 298: 564–566.
Webster, G.C. (1993). Causes, fields, and forms. Acta Biotheoretica (this volume).
Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. theoret. Biol. 25: 1–47.
Wolpert, L. (1989). Positional information revisited. Development 107: Supplement: 3–12.
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Goodwin, B. Homology and a generative theory of biological form. Acta Biotheor 41, 305–314 (1993). https://doi.org/10.1007/BF00709368
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DOI: https://doi.org/10.1007/BF00709368