Abstract
In this article the interface between development and homology is discussed. Development is here interpreted as a sequence of evolutionarily independent stages. Any approach stressing the importance of specific developmental stages is rejected. A homology definition is favoured which includes similarity and complexity serves as a test for homology. Complexity is seen as the possibility of subdividing a character into evolutionarily independent corresponding substructures. Topology as a test for homology is critically discussed because corresponding positions are not necessarily indicative of homology. Complexity can be used twofold for homology assessments of development: either stages or processes of development are homologised. These two approaches must not be conflated. This distinction leads to the conclusion that there is no ontogenetic homology “criterion”.
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References
Alwes, F., Scholtz, G., 2004. Cleavage and gastrulation of the euphausiaceanMeganyctiphanes norvegica (Crustacea, Malacostraca). Zoomorphology 123, 125–137.
Angelini, D.R., Kaufman, T.C., 2005. Insect appendages and comparative ontogenetics. Dev. Biol. (in press).
Ax, P., 1988. Systematik in der Biologie. Gustav Fischer, Stuttgart.
Bang, R., DeSalle, R., Wheeler, W., 2000. Transformationalism, taxism, and developmental biology in systematics. Syst. Biol. 49, 19–27.
Bock, W.J., 1989. The homology concept: its philosophical foundation and practical methodology. Zool. Beitr. (NF) 32, 327–353.
Bolker, J.A., Raff, R.A., 1996. Developmental genetics and traditional homology. BioEssays 18, 489–494.
Boyan, G.S., Williams, J.L.D., 1995. Lineage analysis as an analytical tool in the insect nervous system: bringing order to interneurons. In: Breidbach, O., Kutsch, W. (Eds.), The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. Birkhäuser, Basel, pp. 273–301.
Brigandt, I., 2002. Homology and the origin of causes. Biol. Phil. 17, 389–407.
Brigandt, I., 2003. Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept. J. Exp. Zool. (Mol. Dev. Evol.) 299B, 9–17.
Brower, A.V.Z., Schawaroch, V., 1996. Three steps of homology assessment. Cladistics 12, 265–272.
Conklin, E.G., 1905. Organization and cell-lineage of the ascidian egg. Proc. Acad. Natl. Sci. Philadelphia 13, 1–119.
Davis, G.K., D’Alessio, J.A., Patel, N.H., 2005. Pax3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. Dev. Biol. 285, 169–184.
de Beer, G.R., 1971. Homology, an Unsolved Problem. Oxford University Press, London.
dePinna, M.C.C., 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7, 367–394.
Dickinson, W.J., 1995. Molecules and morphology: where is the homology? TIG 11, 119–121.
Doe, C.Q., 1992. Molecular markers for identified neuroblasts and ganglion mother cells in theDrosophila central nervous system. Development 116, 855–863.
Dohle, W., 1976. Zur Frage des Nachweises von Homologien durch die komplexen Zell- und Teilungsmuster in der embryonalen Entwicklung höherer Krebse (Crustacea, Malacostraca, Peracarida). Sitzber. Ges. Naturf. Freunde Berlin (N.F.) 16, 125–144.
Dohle, W., 1989a. Zur Frage der Homologie ontogenetischer Muster. Zool. Beitr. (N.F.) 32, 355–389.
Dohle, W., 1989b. Differences in cell pattern formation in early embryology and their bearing on evolutionary changes in morphology. Geobios mém. spec. 12, 145–155.
Dohle, W., 1999. The ancestral cleavage pattern of the clitellates and its phylogenetic deviations. Hydrobiologia 402, 267–283.
Dohle, W., 2004. Die Verwandtschaftsbeziehungen der Großgruppen der Deuterostomier: Alternative Hypothesen und ihre Begründung. Sitzber. Ges. Naturf. Freunde Berlin (N.F.) 43, 123–162.
Dohle, W., Gerberding, M., Hejnol, A., Scholtz, G., 2004. Cell lineage, segment differentiation and gene expression in crustaceans. In: Scholtz, G. (Ed.), Evolutionary Developmental Biology of Crustacea. Balkema, Lisse, pp. 95–133.
Donoghue, M.J., Sanderson, M.J., 1994. Complexity and homology in plants. In: Hall, B.K. (Ed.), Homology, the Hierarchical Basis of Comparative Biology. Academic Press, San Diego, pp. 394–421.
Duboule, D., 1994. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate bauplan and the evolution of morphologies through heterochrony. Development (suppl.), 135–142.
Edgecombe, G.D., Richter, S., Wilson, G.D.F., 2003. The mandibular gnathal edges: homologous structures throughout Mandibulata? Afr. Invertebr. 44, 115–135.
Fechter, H., 1971. Manteltiere, Schädellose, Rundmäuler. Walter de Gruyter & Co., Berlin.
Félix, M.-A., De Ley, P., Sommer, R.J., Frisse, L., Nadler, S.A., Thomas, W.K., Vanfleteren, J., Sternberg, P.W., 2000. Evolution of vulva development in the Cephalobina (Nematoda). Dev. Biol. 221, 68–86.
Franz, V., 1927. Ontogenie und Phylogenie. Das sogenannte biogenetische Grundgesetz und die biometabolischen Modi. Abh. Theor. organ. Entw. 3, 1–51.
Galis, F., Metz, J.A.J., 2001. Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. J. Exp. Zool. (Mol. Dev. Evol.) 291, 195–204.
Gegenbaur, C., 1878. Grundriss der vergleichenden Anatomie. Wilhelm Engelmann, Leipzig.
Gehring, W.J., 2004. Historical perspective on the development and evolution of eyes and photoreceptors. Int. J. Dev. Biol. 48, 707–717.
Gerberding, M., Browne, W.E., Patel, N.H., 2002. Cell lineage analysis of the amphipodParhyale hawaiensis reveals and early restriction of cell fates. Development 129, 5789–5801.
Ghiselin, M.T., 1969. The distinction between similarity and homology. Syst. Zool. 18, 148–149.
Gilbert, S.F., Bolker, J.A., 2001. Homologies of process and modular elements of embryonic construction. J. Exp. Zool. (Mol. Dev. Evol.) 291, 1–12.
Grant, T., Kluge, A.G., 2004. Transformation series as an ideographic character concept. Cladistics 20, 23–31.
Greenspan, R.J., 2001. The flexible genome. Nature Rev. Gen. 2, 383–387.
Guralnick, R., 2002. A recapitulation of the rise and fall of the cell lineage research program: the evolutionary-developmental relationship to cleavage to homology, body plants and life history. J. Hist. Biol. 35, 537–567.
Haeckel, E., 1866. Generelle Morphologie der Organismen. Georg Reimer, Berlin.
Hall, B.K. (Ed.), 1994. Homology—The Hierarchical Basis of Comparative Biology. Academic Press, San Diego.
Hall, B.K., 1995. Homology and embryonic development. Evolution. Biol. 28, 1–37.
Hall, B.K., 1999. Evolutionary Developmental Biology, second ed. Kluwer Academic Publishers, Dordrecht.
Haszprunar, G., 1992. The types of homology and their significance for evolutionary biology and phylogenetics. J. Evol. Biol. 5, 13–24.
Hejnol, A., Scholtz, G., 2004. Clonal analysis ofDistal-less andengrailed expression patterns during early morphogenesis of uniramous and biramous crustacean limbs. Dev. Genes Evol. 214, 473–485.
Hennig, W., 1966. Phylogenetic Systematics. University of Illinois Press, Urbana.
Hennig, W., 1982. Phylogenetische Systematik. Paul Parey, Berlin.
Hertzler, P.L., Clark Jr., W.H., 1992. Cleavage and gastrulation in the shrimpSicyonia ingentis. Development 116, 127–140.
Hughes, C.L., Kaufman, T.C., 2002.Hox genes and the evolution of the arthropod body plan. Evol. Dev. 4, 459–499.
Janies, D., DeSalle, R., 1999. Development, evolution, and corroboration. Anat. Rec. 257, 6–14.
Jenner, R.A., Scholtz, G., 2005. Playing another round of metazoan phylogenetics: Historical epistemology, sensitivity analysis, and the position of Arthropoda within the Metazoa on the basis of morphology. In: Koenemann, S., Jenner, R.A. (Eds.), Crustacea and Arthropod Relationships. Taylor & Francis, Boca Raton, pp. 355–385.
Jockusch, E.L., Ober, K.A., 2004. Hypothesis testing in evolutionary developmental biology: a case study from insect wings. J. Hered. 95, 382–396.
Jockusch, E.L., Nulsen, C., Newfeld, S.J., Nagy, L.M., 2000. Leg development in flies versus grasshoppers: differences indpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development 127, 1617–1626.
Katz, P.S., Tazaki, K., 1992. Comparative and evolutionary aspects of the crustacean stomatogastric system. In: Harris-Warrick, R.M., Marder, E., Selverston, A.I., Moulins, M. (Eds.), Dynamic Biological Networks: The Stomatogastric Nervous System. MIT Press, Cambridge, MA, pp. 221–261.
Kluge, A.G., 2003. The repugnant and the mature in phylogenetic inference: atemporal similarity and historical identity. Cladistics 19, 356–368.
Kuo, D.-H., Shankland, M., 2003. A distinct pattern mechanism of O and P cell fates in the development of the rostral segments of the leechHelobdella robusta: implications for the evolutionary dissociation of developmental pathway and morphological outcome. Development 131, 105–114.
Larimer, J.L., Pease, C.M., 1990. Unexpected divergence among identified interneurons in different abdominal segments of the crayfishProcambarus clarkii. J. Exp. Zool. 253, 20–29.
Laubichler, M.D., Maienschein, J., 2003. Ontogeny, anatomy, and the problem of homology: Carl Gegenbaur and the American tradition of cell lineage studies. Theory Biosci. 122, 194–203.
Laugsch, M., Schierenberg, E., 2004. Differences in maternal supply and early development of closely related nematode species. Int. J. Dev. Biol. 48, 655–662.
Lee, P.N., Callaerts, P., de Couet, H.G., Martindale, M.Q., 2003. CephalopodHox genes and the origin of morphological novelties. Nature 424, 1061–1065.
Liu, P.Z., Kaufman, T.C., 2005.Even-skipped is not a pair-rule gene but has segmental and gap-like functions inOncopeltus fasciatus, an intermediate germband insect. Development 132, 2081–2092.
Løvtrup, S., 1978. On von Baerian and Haeckelian recapitulation. Syst. Zool. 27, 348–352.
Mayr, E., 1969. Principles of Systematic Zoology. McGraw-Hill, New York.
Mickoleit, G., 2004. Phylogenetische Systematik der Wirbeltiere. Verlag Dr. Friedrich Pfeil, München.
Mindell, D.P., Meyer, A., 2001. Homology evolving. Tree 16, 434–440.
Minelli, A., 1998. Molecules, developmental modules, and phenotypes: a combinatorial approach to homology. Mol. Phylogen. Evol. 9, 340–347.
Minelli, A., 2003. The Development of Animal Form. Cambridge University Press, Cambridge.
Mittmann, B., 2002. Early neurogenesis in the horseshoe crabLimulus polyphemus and its implication for arthropod phylogeny. Biol. Bull. 203, 221–222.
Mittmann, B., Scholtz, G., 2003. Development of the nervous system in the “head” ofLimulus polyphemus (Chelicerata, Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev. Genes Evol. 213, 9–17.
Mocek, R., 1998. Die werdende Form. Basilisken-Presse, Marburg.
Müller, F., 1864. Für Darwin. Engelmann, Leipzig.
Müller, G.B., Wagner, G.P., 1996. Homology,Hox genes, and developmental biology. Am. Zool. 36, 4–13.
Nielsen, C., 2001. Animal Evolution, second ed. Oxford University Press, Oxford.
Nielsen, C., Martinez, P., 2003. Patterns of gene expression: homology or homocrazy. Dev. Gen. Evol. 213, 149–154.
Oda-Ishii, I., Bertrand, V., Matsuo, I., Lemaire, P., Saiga, H., 2005. Making very similar embryos with divergent genomes: conservation of regulatory mechanisms ofOtx between the ascidiansHalocynthis roretzi andCiona intestinalis. Development 132, 1663–1674.
Osche, G., 1973. Das Homologisieren als eine grundlegende Methode der Phylogenetik. Aufs. Red. Senckenberg. Naturf. Ges. 24, 155–165.
Osche, G., 1982. Rekapitulationsentwicklung und ihre Bedeutung für die Phylogenetik—wann gilt die “Biogenetische Grundregel”? Verh. naturwiss. Ver. Hamburg (N.F.) 25, 5–31.
Panchen, A.L., 1992. Classification, Evolution, and the Nature of Biology. Cambridge University Press, Cambridge.
Panchen, A.L., 1994. Richard Owen and the concept of homology. In: Hall, B.K. (Ed.), Homology—The Hierarchical Basis of Comparative Biology. Academic Press, San Diego, pp. 21–62.
Patel, N.H., Ball, E.E., Goodman, C.S., 1992. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357, 339–342.
Patel, N.H., Condron, B.G., Zinn, K., 1994. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367, 429–434.
Patterson, C., 1982. Morphological characters and homology. In: Joysey, K.A., Friday, A.E. (Eds.), Problems of Phylogenetic Reconstruction. Academic Press, London, pp. 21–74.
Paulus, H., 1996. Euarthropoda. In: Westheide, W., Rieger, R. (Eds.), Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp. 435–444.
Paulus, H.F., 2000. Phylogeny of Myriapoda—Crustacea—Insecta: a new attempt using photoreceptor structure. J. Zool. Syst. Evol. Res. 38, 189–208.
Pearson, K.G., Boyan, G.S., Bastiani, M., Goodman, C.S., 1985. Heterogeneous properties of segmentally homologous interneurons in the ventral nerve cord of locusts. J. Comp. Neurol. 233, 133–145.
Popadic, A., Panganiban, G., Rusch, D., Shear, W.A., Kaufman, T.C., 1998. Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev. Genes Evol. 208, 142–150.
Raff, R.A., 1996. The Shape of Life: Genes, Development, and the Evolution of Animal Form. University of Chicago Press, Chicago.
Raff, R.A., 1999. Larval homologies and radical evolutionary changes in early development. In: Homology (Novartis foundation Symposium 222). Wiley, Chichester, pp. 110–121.
Remane, A., 1952. Die Grundlagen des natürlichen Systems der vergleichenden Anatomie und der Phylogenetik. Geest und Portig, Leipzig.
Remane, A., 1960. Die Beziehungen zwischen Phylogenie und Ontogenie. Zool. Anz. 164, 306–337.
Richardson, M.K., 1999. Vertebrate evolution: the developmental origins of adult variation. BioEssays 21, 604–613.
Richardson, M.K., Hanken, J., Gooneratne, M.L., Pieau, C., Raynaud, A., Selwood, L., Wright, G.M., 1997. There is no highly conserved embryonic stage in the vertebrates, implications for current theories of evolution and development. Anat. Embryol. 196, 91–106.
Richardson, M.K., Allen, S.P., Wright, G.M., Raynaud, A., Hanken, J., 1998. Somite number and vertebrate evolution. Development 125, 151–160.
Richter, S., 2002. The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Org. Divers. Evol. 2, 217–237.
Riedl, R., 1975. Die Ordnung des Lebendigen. Parey, Hamburg.
Riedl, R., 2000. Strukturen der Komplexität. Springer, Berlin.
Rieppel, O.C., 1988. Fundamentals of Comparative Biology. Birkhäuser, Basel.
Rieppel, O., Kearney, M., 2002. Similarity. Biol. J. Linn. Soc. 75, 59–82.
Roth, V.L., 1984. On homology. Biol. J. Linn. Soc. 22, 13–29.
Roth, V.L., 1991. Homology and hierarchies: problems solved and unresolved. J. Evol. Biol. 4, 167–194.
Rudel, D., Sommer, R.J., 2003. The evolution of developmental mechanisms. Dev. Biol. 264, 15–37.
Salthe, S.N., 1993. Development and Evolution—Complexity and Change in Biology. MIT Press, Cambridge.
Sander, K., 1983. The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In: Goodwin, B.C., Holder, N., Wylie, C.G. (Eds.), Development and Evolution. Cambridge University Press, Cambridge, pp. 137–158.
Schmid, A., Chiba, A., Doe, C.Q., 1999. Clonal analysis ofDrosophila embryonic neuroblasts: neural cell types, axon projections and muscular targets. Development 126, 4653–4689.
Schmitt, M., 1995. The homology concept—still alive. In: Breidbach, O., Kutsch, W. (Eds.), The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. Birkhäuser, Basel, pp. 425–438.
Scholtz, G., 1997. Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey, R.A., Thomas, R.H. (Eds.), Arthropod Relationships. Chapman & Hall, London, pp. 317–332.
Scholtz, G., 2000. Evolution of the nauplius stage in malacostracan crustaceans J. Zool. Syst. Evol. Res. 38, 175–187.
Scholtz, G., 2002. The Articulata hypothesis—or what is a segment? Org. Divers. Evol. 2, 197–215.
Scholtz, G., 2004. Baupläne versus ground patterns, phyla versus monophyla: aspects of patterns and processes in evolutionary developmental biology. In: Scholtz, G. (Ed.), Evolutionary Developmental Biology of Crustacea. Balkema, Lisse, pp. 3–16.
Scholtz, G., Dohle, W., 1996. Cell lineage and cell fate in crustacean embryos—a comparative approach. Int. J. Dev. Biol. 40, 211–220.
Scholtz, G., Wolff, G., 2002. Cleavage, gastrulation, and germ disc formation of the amphipodOrchestia cavimana (Crustacea, Malacostraca, Peracarida). Contrib. Zool. 71, 9–28.
Scholtz, G., Mittmann, B., Gerberding, M., 1998. The pattern ofdistal-less expression in the mouthparts of crustaceans, myriapods and insect: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int. J. Dev. Biol. 42, 801–810.
Seidel, F., 1960. Körpergrundgestalt und Keimstruktur: eine Erörterung über die Grundlagen der vergleichenden und experimentellen Embryologie und deren Gültigkeit bei phylogenetischen Überlegungen. Zool. Anz. 164, 245–305.
Seo, H.-C., Edvardsen, R.B., Maeland, A.D., Bjordal, M., Jensen, M.F., Hansen, A., Flaat, M., Weissenbach, J., Lehrach, H., Wincker, P., Reinhard, R. Chourrout, D., 2004.Hox cluster disintegration with persistent anteroposterior order of expression inOikopleura dioica. Nature 431, 67–71.
Sewertzoff, A.N., 1931. Morphologische Gesetzmäßigkeiten der Evolution. Fischer, Jena.
Siewing, R., 1979. Homology of cleavage types? Fortschr. Zool. Syst. Evolutionsforch. 1, 7–18.
Simpson, P., 2002. Evolution of development in closely related species of flies and worms. Nat. Rev. Gen. 3, 907–917.
Simpson, P., Woehl, R., Usui, K., 1999. The development and evolution of bristle patterns in Diptera. Development 125, 1349–1364.
Slack, J.M.W., Holland, P.W.H., Graham, C.F., 1993. The zootype and the phylotypic stage. Nature 361, 490–492.
Spemann, H., 1915. Zur Geschichte und Kritik des Begriffs der Homologie. In: Hinneberg, P. (Ed.), Die Kultur der Gegenwart; Allgemeine Biologie. Teubner, Leipzig, pp. 63–86.
Stark, D., 1979. Vergleichende Anatomie der Wirbeltiere, Band 2: Das Skeletsystem. Springer, Berlin.
Stollewerk, A., Weller, M., Tautz, D., 2001. Neurogenesis in the spiderCupiennius salei. Development 128, 2673–2688.
Strathmann, R.R., 1988. Larvae, phylogeny, and von Baer’s law. In: Paul, C.R.C., Smith, A.B. (Eds.), Echinoderm Phylogeny and Evolutionary Biology. Clarendon Press, Oxford, pp. 53–68.
Striedter, G.F., Northcutt, R.G., 1991. Biological hierarchies and the concept of homology. Brain Behav. Evol. 38, 177–189.
Sudhaus, W., 1980. Problembereiche der Homologienforschung., Verh. Dtsch. Zool. Ges. 73, 177–187.
Sudhaus, W., Rehfeld, K., 1992. Einführung in die Phylogenetik und Systematik. Gustav Fischer, Stuttgart.
Tautz, D., 1992. Redundancies, development and the flow of information. BioEssays. 14, 263–266.
van Valen, L.M., 1982. Homology and causes. J. Morphol. 173, 305–312.
von Baer, K.E., 1828. Ueber Entwickelungsgeschichte der Thiere. Bornträger, Königsberg.
von Baer, K.E., 1873. Entwickelt sich die Larve der einfachen Ascidien in der ersten Zeit nach dem Typus der Wirbelthiere? Mém. Acad. Imp. Sci. St. Pétersbourg 19, 1–35.
Wägele, J.-W., 2005. Foundations of Phylogenetic Systematics. Verlag Dr. Friedrich Pfeil, München.
Wagner, G.P., 1989. The biological homology concept. Ann. Rev. Ecol. Syst. 20, 51–69.
Wagner, G.P., Misof, B. Y., 1993. How can a character be developmentally constrained despite variation in developmental pathways? J. Evol. Biol. 6, 449–455.
Whitington, P.M., 2004. The development of the crustacean nervous system. In: Scholtz, G. (Ed.), Evolutionary Developmental Biology of Crustacea. Balkema, Lisse, pp. 135–167.
Wilson, E.B., 1894. The embryological criterion of homology. In: Biological Lectures Delivered at the Marine Biological Laboratory of Wood’s Hole. Ginn & Co., Boston, pp. 101–124.
Wray, G.A., 1999. Evolutionary dissociations between homologous genes and homologous structures. In: Homology (Novartis foundation Symposium 222). Wiley, Chichester, pp. 189–203.
Wray, G.A., Abouheif, E., 1998. When is homology not homology? Curr. Opin. Gen. Dev. 8, 675–680.
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From the 46th “Phylogenetisches Symposium”, Jena, Germany, November 20–21, 2004. Theme of the symposium: “Evolutionary developmental biology—new challenges to the homology concept?”
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Scholtz, G. Homology and ontogeny: pattern and process in comparative developmental biology. Theory Biosci. 124, 121–143 (2005). https://doi.org/10.1007/BF02814480
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DOI: https://doi.org/10.1007/BF02814480