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7 - The developmental evolution of avian digit homology: an update

Published online by Cambridge University Press:  28 June 2009

By
Günter P. Wagner
Edited by
Manfred D. Laubichler  and
Jane Maienschein
Manfred D. Laubichler
Affiliation:
Arizona State University
Jane Maienschein
Affiliation:
Arizona State University
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Summary

INTRODUCTION

It is a truism of evolutionary developmental biology that the evolution of phenotypic characters has to be caused by the evolutionary modification of their developmental pathways (Hall 1998; Raff 1996). Surprisingly, however, the evolutionary conservation of a phenotypic character does not imply the conservation of its developmental pathway (Hall 1994; Wagner and Misof 1993; Weiss and Fullerton 2000). A paradigmatic case of this problem is the homology of the digits in the bird wing. Phylogenetic evidence conclusively shows that the digits of the bird wing are the thumb, the index finger, and the middle finger – that is, digits DI, DII, and DIII (Sereno 1999b). The embryological origin of these fingers, however, is identical to that of those fingers that usually form the index, middle, and “ring” finger – that is, digits DII, DIII, and DIV (Burke and Feduccia 1997; Hinchliffe and Hecht 1984; Müller and Alberch 1990). This discrepancy has been unresolved since the discovery of the dinosaur affinities of birds in the mid nineteenth century, and it continues to fuel a heated debate among paleontologists, ornithologists, and developmental biologists (Feduccia 1996, 1999, 2001; Galis et al. 2003; Prum 2002). Furthermore, it created a discrepancy in the naming of the wing digits between the evolutionary literature and the considerable number of papers in molecular developmental biology, because the chick wing is an important model system.

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Form and Function in Developmental Evolution , pp. 153 - 175
Publisher: Cambridge University Press
Print publication year: 2009

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References

Amundson, R. (2005). The Changing Role of the Embryo in Evolutionary Thought: Roots of Evo-Devo. Cambridge University Press.CrossRefGoogle Scholar
Benedetto, J. L. (1973). Herrerasauridae, nueva familia de sarisquios triscos. Ameghiniana 10, 89–102.Google Scholar
Brandley, M. C., Schmitz, A., and Reader, T. (2005). Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology 54, 373–90.CrossRefGoogle ScholarPubMed
Braus, H. (1906). Die Entwicklung der Form der Extremitäten und des Extremitätenskeletts. In Hertwig, O. (ed.), Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere. Jena: Gustav Fisher, vol. III, part 2, pp. 167–338.Google Scholar
Bruno, S. and Maugeri, S. (1976). Rettili d'Italia: Tartarughe e Sauri. Florence: I. A. Martello.Google Scholar
Burke, A. C. and Alberch, P. (1985). The development and homology of the chelonian carpus and tarsus. Journal of Morphology 186, 119–31.CrossRefGoogle Scholar
Burke, A. C. and Feduccia, A. (1997). Developmental patterns and the identification of homologies in the avian hand. Science 278, 666–8.CrossRefGoogle Scholar
Caputo, V., Lanza, B., and Palmieri, R. (1995). Body elongation and limb reduction in the genus Chalcides Laurenti 1768 (Squamata Scincidae): a comparative study. Tropical Zoology 8, 95–152.CrossRefGoogle Scholar
Carroll, S. B., Grenier, J. K., and Weatherbee, S. D. (2001). From DNA to Diversity. Malden, MA: Blackwell Science.Google Scholar
Chatterjee, S. (1998). Counting the fingers of birds and dinosaurs. Science 280, 355a.CrossRefGoogle Scholar
Colbert, E. (1970). A saurischian dinosaur from the Triassic of Brazil. American Museum Novitates 2405, 1–39.Google Scholar
Dahn, R. D. and Fallon, J. F. (2000). Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289, 438–41.CrossRefGoogle ScholarPubMed
Dunlop, L. -L. T. and Hall, B. K. (1995). Relationships between cellular condensation, preosteoblast formation and epithelial-mesenchymal interactions in initiation of osteogenesis. International Journal of Developmental Biology 39, 357–71.Google ScholarPubMed
Fabrezi, M. (2001). A survey of prepollex and prehallux variation in anuran limbs. Zoological Journal of the Linnean Society 131, 227–48.CrossRefGoogle Scholar
Feduccia, A. (1996). The Origin and Evolution of Birds. New Haven: Yale University Press.Google Scholar
Feduccia, A. (1999). 1,2,3 = 2,3,4: accommodating the cladogram. Proceedings of the National Academy of Sciences USA 96, 4740–2.CrossRefGoogle ScholarPubMed
Feduccia, A. (2001). Digit homology of birds and dinosaurs: accommodating the cladogram. Trends in Ecology & Evolution 16, 285–6.CrossRefGoogle ScholarPubMed
Feduccia, A. and Nowicki, J. (2002). The hand of birds revealed by early ostrich embryos. Naturwissenschaften 89, 391–3.CrossRefGoogle ScholarPubMed
Fürbringer, M. (1870). Die Knochen und Muskeln der Extremitäten bei den schlangenähnlichen Sauriern: vergleichend anatomische Abhandlung. Leipzig: Verlag von Wilhelm Engelmann.CrossRefGoogle Scholar
Galis, F., Kundrát, M., and Metz, J. A. J. (2005). Hox genes, digit identities and the theropod/bird transition. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 304B, 198–205.CrossRefGoogle Scholar
Galis, F., Kundrát, M., and Sinervo, B. (2003). An old controversy solved: bird embryos have five fingers. Trends in Ecology & Evolution 18, 7–9.CrossRefGoogle Scholar
Garner, J. P. and Thomas, A. L. R. (1998). Counting the fingers of birds. Science 280, 355.Google Scholar
Gauthier, J. (1986). Saurischian monophyly and the origin of birds. Memoirs of the California Academy of Science 8, 1–55.Google Scholar
Grandel, H. and Schulte-Merker, S. (1998). The development of the paired fins in the Zebrafish (Danio rerio). Mechanisms of Development 79, 99–120.CrossRefGoogle Scholar
Greer, A. E. (1991). Limb reduction in Squamates: identification of the lineages and discussion of the trends. Journal of Herpetology 25, 166–73.CrossRefGoogle Scholar
Greer, A. E., Caputo, V., Lanza, B., and Palmieri, R. (1998). Observations on limb reduction in the scincid lizard genus Chalcides. Journal of Herpetology 32, 244–52.CrossRefGoogle Scholar
Hall, B. K. (1994). Homology and embryonic development. In Hecht, M. K., MacIntyre, R. J., and Clegg, M. T. (eds.), Evolutionary Biology. New York: Plenum Press, vol. XXVIII, pp. 1–30.Google Scholar
Hall, B. K. (1998). Evolutionary Developmental Biology. London: Chapman and Hall.Google Scholar
Hall, B. K. and Miyake, T. (1995). Divide, accumulate, differentiate: cell condensation in skeletal development revisited. International Journal of Developmental Biology 39, 881–93.Google ScholarPubMed
Hess, H. (1957). Beiderseitige kongenitale daumenlose Fünffingerhand bei Mutter und Kind. Zeitschrift für Anatomie und Entwicklungsgeschichte 120, 226–31.CrossRefGoogle Scholar
Hinchliffe, J. R. (1977). The chondrogenic pattern in chick limb morphogenesis: a problem of development and evolution. In Ede, D. A., Hinchliffe, J. R., and Balls, M. (eds.), Vertebrate Limb and Somite Morphogenesis. Cambridge University Press, pp. 293–309.Google Scholar
Hinchliffe, J. R. and Griffiths, P. J. (1983). The prechondrogenic patterns in tetrapod limb development and their phylogenetic significance. In Goodwin, B. C., Holder, N., and Wylie, C. C. (eds.), Development and Evolution. Cambridge University Press, pp. 99–121.Google Scholar
Hinchliffe, J. R. and Hecht, M. (1984). Homology of the bird wing skeleton. Evolutionary Biology 20, 21–37.CrossRefGoogle Scholar
Hinchliffe, J. R. and Johnson, D. R. (1980). The Development of the Vertebrate Limb. New York: Oxford University Press.Google Scholar
Hiraki, Y. and Shukunami, C. (2000). Chondromodulin-I as a novel cartilage-specific growth-modulating factor. Pediatric Nephrology 14, 602–5.CrossRefGoogle ScholarPubMed
Holtz, T. R., Jr. (1995). A new phylogeny of the Theropoda. Journal of Vertebrate Paleontology 15, 35A.Google Scholar
Joachimsthal, G. (1900). Verdoppelung des linken Zeigefingers und Dreigliederung des rechten Daumens. Berliner Klinische Wochenschrift 37, 835–8.Google Scholar
Kundrát, M. and Seichert, V. (2001). Developmental remnants of the first avian metacarpus. Journal of Morphology 248, 252A.Google Scholar
Kundrát, M., Seichert, V., Russell, A. P., and Smetana, K., Jr. (2002). Pentadactyl pattern of the avian wing autopodium and pyramid reduction hypothesis. Journal of Experimental Zoology Mol Dev Evol 294, 152–9.Google ScholarPubMed
Larsson, H. C. E. and Wagner, G. P. (2002). The pentadactyl ground state of the avian wing. Journal of Experimental Zoology Mol Dev Evol 294, 146–51.CrossRefGoogle ScholarPubMed
Litingtung, Y., Dahn, R. D., Li, Y., Fallon, J. F., and Chiang, C. (2002). Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418, 979–83.CrossRefGoogle ScholarPubMed
Montagna, W. (1945). A re-investigation of the development of the wing of the bird. Journal of Morphology 76, 87–118.CrossRefGoogle Scholar
Müller, G. B. and Alberch, P. (1990). Ontogeny of the limb skeleton in Alligator mississippiensis: developmental invariance and change in the evolution of Archosaur limbs. Journal of Morphology 203, 151–64.CrossRefGoogle Scholar
Novas, F. E. (1993). New information on the systematics and postcranial skeleton of Herrerasaurus ischigualastensis (Theropoda: Herrerasauridae) from the Ischigualasto formation (Upper Triassic) of Argentina. Journal of Vertebrate Paleontology 13, 400–23.CrossRefGoogle Scholar
Novas, F. E. (1997). Herrerasauridae. In Currie, P. J. and Padian, K. (eds.), Encyclopedia of Dinosaurs. San Diego: Academic Press, pp. 303–11.Google Scholar
Nyhart, L. K. (1995). Biology Takes Form. Animal Morphology and the German Universities, 1800–1900. University of Chicago Press.Google Scholar
Nyhart, L. K. (2002). Learning from history: morphology's challenges in Germany ca 1900. Journal of Morphology 252, 2–14.CrossRefGoogle ScholarPubMed
Orsini, J. -P. and Cheylan, M. (1981). Chalcides chalcides (Linnaeus 1758) – Erzschleiche. In Böhme, W. (ed.), Handbuch der Reptilien und Amphibien Europas. Wiesbaden: Akademische Verlagsgesellschaft, vol. I, pp. 318–37.Google Scholar
Padian, K. (1992). A proposal to standardize tetrapod phalangeal formula designations. Journal of Vertebrate Paleontology 12, 260–2.CrossRefGoogle Scholar
Padian, K. and May, C. L. (1993). The earliest dinosaurs. New Mexico Museum of Natural History and Science Bulletin 3, 379–81.Google Scholar
Prum, R. O. (2002). Why ornithologists should care about the theropod origin of birds. The Auk 119, 1–17.CrossRefGoogle Scholar
Qazi, Q. and Kassner, E. G. (1988). Triphalangeal thumb. Journal of Medical Genetics 25, 505–20.CrossRefGoogle ScholarPubMed
Raff, R. (1996). The Shape of Life. University of Chicago Press.Google Scholar
Raynaud, A. and Clergue-Gazeau, M. (1986). Identification des doigts réduits ou manquants dans les pattes des embryons de Lézard vert (Lacerta viridis) traités par la cystosine-arabinofuranoside. Comparaison avec les réductions digitales naturelles des espèces de reptiles serpentiformes. Archives de biologie (Bruxelles) 97, 279–99.Google Scholar
Raynaud, A., Clergue-Gazeau, M., and Brabet, J. (1986). Remarques preliminaires sur la structure de la patte du Seps Tridactyle (Chalcides chalcides, L.). Bull Soc Hist Nat, Toulouse 122, 109–11.Google Scholar
Reig, O. A. (1963). La presencia de dinosaurios saurisquios en los “Estratos de Ischigualasto” (Mesotriásico superior) de las provincias de San Juan y La Rioja (República Argentina). Ameghiniana 3, 3–20.Google Scholar
Renous-Lecuru, S. (1973). Morphologie comparée du carpe chez les Lepidosauriens actuels (Rhynchocéphales, Lacertilens, Amphisbéniens). Gegenbaurs morph Jahrb, Leipzig 119, 727–66.Google Scholar
Riddle, R. D., Johnson, R. L., Lauger, E., and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–16.CrossRefGoogle ScholarPubMed
Schwarzbach, M. (1980). Alfred Wegener und die Drift der Kontinente. Stuttgart: Wissenschaftliche Verlagsgesellschaft.Google Scholar
Seichert, V. and Rychter, Z. (1972). Vascularization of developing anterior limb of the chick embryo II. Differentiation of vascular bed and its significance for the location of morphogenetic processes inside the limb bud. Folia Morphologica (Warsz) 19, 352–61.Google Scholar
Sereno, P. (1994). The pectoral girdle and forelimb of the basal theropod Herrerasaurus ischigualestensis. Journal of Vertebrate Paleontology 13(4), 425–50.CrossRefGoogle Scholar
Sereno, P. C. (1993). Dinosaurian precursors from the Middle Triassic of Argentina: Lagerpeton chanarensis. Journal of Vertebrate Paleontology 13, 385–99.CrossRefGoogle Scholar
Sereno, P. C. (1999a). A rationale for dinosaurian taxonomy. Journal of Vertebrate Paleontology 19, 788–90.CrossRefGoogle Scholar
Sereno, P. C. (1999b). The evolution of dinosaurs. Science 284, 2137–47.CrossRefGoogle ScholarPubMed
Sereno, P. C., Forster, C. A., Rogers, R. R., and Monetta, A. M. (1993). Primitive dinosaur skeleton from Argentina and the early evolution of Dinosauria. Nature 361, 64–6.CrossRefGoogle Scholar
Sereno, P. C. and Novas, F. E. (1992). The complete skull and skeleton of an early dinosaur. Science, 258, 1137–40.CrossRefGoogle ScholarPubMed
Sewertzoff, A. N. (1931). Studien über die Reduktion der Organe der Wirbeltiere. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 53, 611–99.Google Scholar
Shubin, N. H. (1994). The phylogeny of development and the origin of homology. In Grande, L. and Rieppel, O. (eds.), Interpreting the Hierarchy of Nature. San Diego: Academic Press.Google Scholar
Shubin, N. H. and Alberch, P. (1986). A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evolutionary Biology 20, 319–87.Google Scholar
Steiner, H. (1934). Über die embryonale Hand- und Fuss-Skelettanlage bei den Crocodiliern, sowie über ihre Beziehung zur Vogel-Flügelanlage und zur ursprünglichen Tetrapoden-Extremität. Revue Suisse de Zoologie 41, 383–96.CrossRefGoogle Scholar
Steiner, H. and Anders, G. (1946). Zur Frage der Entstehung von Rudimenten. Die Reduktion der Gliedmassen von Chalcides tridactylus Laur. Revue Suisse de Zoologie 53, 537–46.Google Scholar
Swanson, A. B. and Brown, K. S. (1962). Hereditary triphalangeal thumb. Journal of Heredity 53, 259–65.CrossRefGoogle Scholar
Vargas, A. and Fallon, J. F. (2005). Birds have dinosaur wings: the molecular evidence. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 304B, 86–90.CrossRefGoogle Scholar
Vargas, A. O., Kohlsdorf, T., Fallon, J. F., VandenBrooks, J., and Wagner, G. P. (2008). The evolution of HoxD-11 expression in the bird wing: insights fromAlligator mississippiensis. PLo S ONE 3, e3325.Google Scholar
Wagner, G. P. and Gauthier, J. A. (1999). 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Sciences 96, 5111–16.CrossRefGoogle ScholarPubMed
Wagner, G. P. and Misof, B. Y. (1993). How can a character be developmentally constrained despite variation in developmental pathways?Journal of Evolutionary Biology 6, 449–55.CrossRefGoogle Scholar
Warm, A., Di Pietro, C., D.’Agrosa, F., Gamblé, M., and Gaboardi, F. (1988). Non-opposable triphalangeal thumb in an Italian family. Journal of Medical Genetics 25, 337–9.CrossRefGoogle Scholar
Weiss, K. M. and Fullerton, S. M. (2000). Phenotypic drift and the evolution of genotype–phenotype relationships. Theoretical Population Biology 57, 187–95.CrossRefGoogle Scholar
Welscher, P. te., Zuniga, A., Kuijper, S., Drenth, T., Goedemans, H. J., Meijlink, F., and Zeller, R. (2002). Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298, 827–30.CrossRefGoogle Scholar
Welten, M. C. M., Verbeek, F. J., Meijer, A. H., and Richardson, M. K. (2005). Gene expression and digit homology in the chicken embryo wing. Evolution & Development 7, 18–28.CrossRefGoogle ScholarPubMed
Zschabitz, A. (1998). Glycoconjugate expression and cartilage development of the cranial skeleton. Acta Anatomica 61, 254–74.CrossRefGoogle Scholar

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