• Please log in or register to access this feature.

Special Issue Reviews–A Peer Reviewed Forum

You have free access to this content

Identity of the avian wing digits: Problems resolved and unsolved†

  1. Rebecca L. Young1,*,
  2. Gabe S. Bever2,
  3. Zhe Wang1,
  4. Günter P. Wagner1

Article first published online: 15 MAR 2011

DOI: 10.1002/dvdy.22595

Issue

Developmental Dynamics

Developmental Dynamics

Special Issue: Special Issue on Limb Development

Volume 240, Issue 5, pages 1042–1053, May 2011

Additional Information

How to Cite

Young, R. L., Bever, G. S., Wang, Z. and Wagner, G. P. (2011), Identity of the avian wing digits: Problems resolved and unsolved. Dev. Dyn., 240: 1042–1053. doi: 10.1002/dvdy.22595

Author Information

  1. 1

    Yale Systems Biology Institute, Department of Ecology and Evolutionary Biology, Yale University, West Haven, Connecticut

  2. 2

    Department of Geology and Geophysics, Yale University, New Haven, Connecticut

*Yale Systems Biology Institute, Department of Ecology and Evolutionary Biology, Yale University, 300 Heffernan Drive, West Haven, CT 06516

  1. †

    In keeping with the traditional nomenclature, Arabic numerals (1–5) will be used when referring to the embryological position of a digit in the developing autopod regardless of the digit's terminal identity. Roman numerals (I–V) will be used when referring to digit identity.

Publication History

  1. Issue published online: 20 APR 2011
  2. Article first published online: 15 MAR 2011
  3. Manuscript Accepted: 30 JAN 2011

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (449K)

REFERENCES

  • Alberch P, Gale EA. 1985. A developmental analysis of an evolutionary trend: digit reduction in amphibians. Evolution 39: 8–23.
  • Benazet J-D, Bischofberger M, Tiecke E, Goncalves A, Martin JF, Zuniga A, Naef F, Zeller R. 2009. A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323: 1050–1053.
  • Bever GS, Gauthier JA, Wagner GP. 2011. Finding the frameshift: digit loss, developmental variability, and the origin of the avian hand. Evol Dev (in press).
  • Burke AC, Alberch P. 1985. The development and homology of the chelonian carpus and tarsus. J Morphol 186: 119–131.
    Direct Link:
  • Burke AC, Feduccia A. 1997. Developmental patterns and the identification of homologies in the avian hand. Science 278: 666–668.
  • Caputo V, Lanza B, Palmieri R. 1995. Body elongation and limb reduction in the genus Chalcides Laurenti, 1768 (Squamata: Scincidae). Trop Zool 8: 95–152.
  • Carrano M, Sampson SD. 2008. The phylogeny of Ceratosauria (Dinosauria Theropoda). J Syst Palaeontol 6: 183–236.
  • Chatterjee S. 1998. Counting the fingers of birds and dinosaurs. Science 280: 355.
  • Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, Beachy PA, Fallon JF. 2001. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev Biol 236: 421–435.
  • Clark JM, Norell MA, Chiappe LM. 2002. Cladistic approaches to bird orgins. In: ChiappeLM, WitmerLM, editors. Mesozoic birds: above the heads of dinosaurs. Berkeley, CA: University of California Press. p 31–61.
  • Coria RA, Chiappe LM, Dingus L. 2002. A new close relative of Carnotaurus sastrei Bonaparte 1985 (Theropoda: Abelisauridae) from the Late Cretaceous of Patagonia. J Vertebr Paleontol 22: 160–465.
  • Currie PJ, Zhao X-J. 1993. A new carnosaur (Dinosauria, Theropoda) from the Jurassic of Xinjiang, People's Republic of China. Can J Earth Sci 30: 2037–2081.
  • Dahn RD, Fallon JF. 2000. Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289: 438–441.
  • Fabrezi M. 2001. A survey of prepollex and prehallux variation in anuran limbs. Zool J Linn Soc 131: 227–248.
    Direct Link:
  • Feduccia A. 1996. The origin and evolution of birds. New Haven: Yale University Press.
  • Feduccia A. 1999. 1,2,3 = 2,3,4: accommodating the cladogram. Proc Natl Acad Sci U S A 96: 4740–4742.
  • Fürbringer M. 1870. Die Knocken und Muskeln der Extremitäten bei den shlangernähnlichen Sauriern: Vergleichend Anatomische Abhandlung. Leipzig: Verlag von Wilhelm Engelmann.
  • Galis F, Kundrát M, Sinervo B. 2003. An old controversy solved: bird embryos have five fingers. Trends Ecol Evol 18: 7–9.
  • Galis F, Kundrát M, Metz JAJ. 2005. Hox genes, digit identities and the theropod/bird transition. J Exp Zool Mol Dev Evol 304B: 198–205.
    Direct Link:
  • Galis F, van Alphen JJM, Metz JAJ. 2001. Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol Evol 16: 637–646.
  • Galton PM, Upchurch P. 2004. Prosauropoda. In: WeishampelDB, DodsonP, OsmolskaH, editors. The Dinosauria. Berkeley: University of California Press. p 232–258.
  • Garner JP, Thomas ALR. 1998. Counting the fingers of birds. Science 280: 355.
  • Gauthier JA. 1986. Saurischian monophyly and the origin of birds. In: PadianK, editor. The origin of birds and the evolution of flight. San Francisco: California Academy of Sciences. p 1–55.
  • Gauthier JA, de Queiroz K. 2001. Feathered dinosaurs, flying dinosaurs, crown dinosaurs, and the name “Aves”. In: GauthierJA, GallLF, editors. New perspectives on the origin and early evolution of birds: proceedings of the international symposium in honor of John H. Ostrom. New Haven, CT: Peabocy Museum of Natural History, Yale University. p 7–41.
  • Gegenbaur C. 1863. Vergleichendend-anatomische Bermerkungen über das Fusselket der Vögel. Arch Anat Physiol Wiss Med 1863: 450–472.
  • Gonzalez F, Duboule D, Spitz F. 2007. Transgenic analysis of Hoxd gene regulation during digit development. Dev Biol 306: 847–859.
  • Greer AE. 1990. Limb reduction in the scincid lizard genus Lerista. 2. Variation in the bone complements of the front and rear limbs and the number of postsacral vertebrae. J Herpetol 24: 142–150.
  • Greer AE. 1991. Limb reduction in squamates: identification of the lineages and discussion of the trends. J Herpetol 25: 166–173.
  • Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ. 2004. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118: 517–528.
  • Hinchliffe JR. 1985. “One, two, three” or “two, three, four”: an embryologist's view of the homologies of the digits and carpus of modern birds. In: HechtMK, OstromJH, ViohlG, WellnhoferP, editors. The beginnings of birds. Eichstätt: Freunde des Jura Museums. p 141–147.
  • Hinchliffe JR, Griffiths PJ. 1983. The prechondrogenic patterns in tetrapod limb development and their phylogenetic significance. In: GoodwinBC, HolderN, WylieCC, editors. Development and evolution. Cambridge: University Press. p 99–121.
  • Hinchliffe JR, Hecht MK. 1984. Homology of the bird wing skeleton: embryological versus palaeontological evidence. Evol Biol 30: 21–39.
  • Holder N. 1983. Developmental constraints and the evolution of vertebrate digit patterns. J Theor Biol 104: 451–471.
  • Huxley TH. 1868. On the animals that are most nearly intermediate between birds and reptiles. Ann Mag Nat Hist 4: 66–75.
  • Incardona JP, Gaffield W, Kapur RP, Roelink H. 1998. The teratogenic Veratum aldaloid cyclopmaine inhibits Sonic hedgehog signal transduction. Development 125: 3553–3562.
  • Johnson RL, Tabin CJ. 1997. Molecular models for vertebrate limb development. Cell 90: 979–990.
  • Knezevic V, De Santo R, Schughart K, Huffstadt U, Chiang C, Mahon K, Mackem S. 1997. Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop. Development 124: 4523–4536.
  • Kundrát M. 2009. Primary chondrification foci in the wing basipodium of Struthio camelus with comments on interpretation of autopodial elements in Crocodilia and Aves. J Exp Zool Mol Dev Evol 312B: 30–41.
    Direct Link:
  • Kundrát M, Seichert V, Russell AP, Smetana K. 2002. Pentadactyl pattern of the avian wing autopodium and pyramid reduction hypothesis. J Exp Zool 294: 152–159.
    Direct Link:
  • Larsson HCE, Wagner GP. 2002. Pentadactyl ground state of the avian wing. J Exp Zool 294: 146–151.
    Direct Link:
  • Larsson HC, Heppleston AC, Elsey RM. 2010. Pentadactyl ground state of the manus of Alligator mississippiensis and insights into the evolution of digital reduction in Archosauria. J Exp Zool Mol Dev Evol 314B: 571–579.
    Direct Link:
  • Leal F, Tarazona OA, Ramirez-Pinilla MP. 2010. Limb development in the gekkonid lizard gonatodes albogularis: a reconsideration of homology in the lizard carpus and tarsus. J Morphol 271: 1328–1341.
    Direct Link:
  • Litingtung Y, Dahn RD, Li Y, Fallon JF, Chiang C. 2002. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418: 979–983.
  • Martinez RN, Sereno PC, Alcober OA, Colombi CE, Renne PR, Montanez, Currie BS. 2011. A basal dinosaur from the dawn of the dinosaur era in southwestern Pangaea. Science 331: 206–210.
  • McGlinn E, Tabin CJ. 2006. Mechanistic insight into how Shh patterns the vertebrate limb. Curr Opin Genetics Dev 16: 426–432.
  • Montavon T, Le Garrec J-F, Kerszberg M, Duboule D. 2008. Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes Dev 22: 346–359.
  • Morgan BA, Izpisua-Belmonte JC, Duboule D, Tabin CJ. 1992. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358: 236–239.
  • Morse ES. 1872. On the tarsus and carpus of birds. Ann Lyceum Nat Hist N Y 10: 141–158.
    Direct Link:
  • Müller GB, Alberch P. 1990. Ontogeny of the limb skeleton in Alligator mississippiensis - developmental invariance and change in the evolution of archosaur limbs. J Morphol 203: 151–164.
    Direct Link:
  • Nesbitt SJ, Smith ND, Irmis RB, Turner AH, Downs A, Norell MA. 2009. A complete skeleton of a Late Triassic saurischian and the early evolution of dinosaurs. Science 326: 1530–1533.
  • Norell MA, Xu X. 2005. Feathered dinosaurs. Ann Rev Earth Planet Sci 33: 277–299.
  • Orsini J-P, Cheylan M. 1981. Chalcides chalcides (Linnaeus 1758)–Erzschleiche. In: BöhmeW, editor. Handbuch der Reptien und Amphibien Europas. Wiesbaden: Akademische Verlagsgesellschaft. p 318–337.
  • Oster GF, Shubin N, Murray JD, Alberch P. 1988. Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 42: 862–884.
  • Prum RO. 2002. Why ornithologists should care about the theropod origins of birds. Auk 119: 1–17.
  • Qazi Q, Kassner EG. 1988. Triphalangeal thumb. J Med Genet 25: 505–520.
  • Reno PL, McCollum MA, Cohn MJ, Meindl RS, Hamrick M, Lovejoy CO. 2008. Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories. J Exp Zool Mol Dev Evol 310B: 240–258.
    Direct Link:
  • Renous-Lecuru S. 1973. Morphologie comparee du carge chez les Lepidosauriens actuels (Rhynchocephales, Lacertilens, Amphisbeniens). Gegenbaurs Morphol Jahrb 119: 727–766.
  • Riddle RD, Johnson RL, Laufer E, Tabin C. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401–1416.
  • Rieppel O. 1992. Studies on skeletal formation in reptiles III: patterns of ossification in the skeleton of Lacerta vivipara (Reptilia, Squamata). Fieldiana Zool 68: 1–25.
  • Romer AS, Parsons TS. 1970. The vertebrate body. 4th ed. Philadelphia: WB Saunders.
  • Ros MA, Dahn RD, Fernandez-Teran M, Rashka K, Caruccio NC, Hasso SM, Bitgood J, Lancman JJ, Fallon JF. 2003. The chick oligozeugodactyly (ozd) mutant lacks sonic hedgehog function in the limb. Development 130: 527–537.
  • Roth VL. 1988. The biological basis of homology. In: HumphriesCJ, editor. Onotogeny and systematics. New York: Columbia University Press. p 1–26.
  • Satoh A, Endo T, Abe M, Yakushiji N, Ohgo S, Tamura K, Ide H. 2006. Characterization of Xenopus digits and regenerated limbs of the froglet. Dev Dyn 235: 3316–3326.
    Direct Link:
  • Scherz PJ, McGlinn E, Nissim S, Tabin CJ. 2007. Extended exposure to sonic hedgehog is required for patterning the posterior digits of the vertebrate limb. Dev Biol 308: 343–354.
  • Sereno PC. 1993. Dinosaurian precursors from the Middle Triassic of Argentina: Lagerpeton chanarensis. J Vertebr Paleontol 13: 385–399.
  • Sereno PC. 1994. The pectoral girdle and forelimb of the basal theropod Herrerasaurus ischigualastensis. J Vertebr Paleontol 13: 425–450.
  • Sereno PC. 1997. The origin and evolution of dinosaurs. Ann Rev Earth Planet Sci 25: 435–489.
  • Sereno PC. 1999. The evolution of dinosaurs. Science 284: 2137–2147.
  • Sewertzoff AN. 1931. Studien über die Reduktion der Organe der Wirbeltiere. Zoologische Jahrbucher. Abteilung fur Anatomic und Ontogenie der Tiere, Jena 53: 611–699.
  • Shapiro MD. 2002. Developmental morphology of limb reduction in Hemiergis (squamata: scincidae): chondrogenesis, osteogenesis, and heterochrony. J Morphol 254: 211–231.
    Direct Link:
  • Shapiro MD, Hanken J, Rosenthal N. 2003. Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. J Exp Zool Mol Dev Evol 297B: 48–56.
    Direct Link:
  • Shubin NH. 1994. The phylogeny of development and the origin of homology. In: GrandeL, RieppelO, editors. Interpreting the hierarchy of nature. San Diego: Academic Press. p 210–225.
  • Shubin NH, Alberch P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evol Biol 20: 319–387.
  • Spitz F, Gonzalez F, Duboule D. 2003. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113: 405–417.
  • Steiner H, Anders G. 1946. Zur Frage der Entstehung von Rudimenten. Die Redukction der Gliedmassen von Chalcides tridactylus Laur. Rev Suisse Zool 53: 537–546.
  • Suzuki T, Hasso SM, Fallon JF. 2008. Unique SMAD1/5/8 activity at the phalanx-forming region determines digit identity. Proc Natl Acad Sci U S A 105: 4185–4190.
  • Tamura K, Yonei-Tamura S, Nomura N, Yokoyama H, Seki R. 2011. Embryological evidence identifies wing digits in bird as digits 1, 2, and 3. Science (in press).
  • te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans HJ, Meijlink F, Zeller R. 2002. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298: 827–830.
  • Tickle C, Summerbell D, Wolpert L. 1975. Positional signalling and specification of digits in chick limb morphogenesis. Nature 254: 199–202.
  • Towers M, Mahood R, Yin Y, Tickle C. 2008. Integration of growth and specification in chick wing digit-patterning. Nature 452: 882–886.
  • Turner AH, Pol D, Clarke GM, Erickson GM, Norell MA. 2001. A basal dromaeosaurid and size evolution preceding flight. Science 317: 1378–1381.
  • Uejima A, Amano T, Nomura N, Noro M, Yasue T, Shiroishi T, Ohta K, Yokoyama H, Tamura K. 2010. Anterior shift in gene expression precedes anteriormost digit formation in amniote limbs. Dev Growth Differ 52: 223–234.
    Direct Link:
  • Vargas AO, Fallon JF. 2005a. Birds have dinosaur wings: the molecular evidence. J Exp Zool Mol Dev Evol 304B: 86–90.
    Direct Link:
  • Vargas AO, Fallon JF. 2005b. The digits of the wing of birds are 1, 2, and 3. A review. J Exp Zool Mol Dev Evol 304B: 206–219.
    Direct Link:
  • Vargas AO, Wagner GP. 2009. Frame-shifts of digit identity in bird evolution and cyclopamine-treated wings. Evol Dev 11: 163–169.
    Direct Link:
  • Vargas AO, Kohlsdorf T, Fallon JF, VandenBrooks J, Wagner GP. 2008. The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis. PLoS One 3: e3325.
  • Vargas AO, Wagner GP, Gauthier JA. 2009. Limusaurus and bird digit identity. Nature Proceedings. http://nucleodecenio.blogspot.com/2009/10/limusaurus-and-bird-digit-identity.html.
  • Wada N, Javidan Y, Nelson S, Carney TJ, Kelsh RN, Schilling TF. 2005. Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 132: 3977–3988.
  • Wagner GP. 2005. The developmental evolution of avian digit homology: an update. Theory Biosci 124: 165–183.
  • Wagner GP. 2007. The developmental genetics of homology. Nat Rev Genet 8: 473–479.
  • Wagner GP, Gauthier JA. 1999. 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proc Natl Acad Sci U S A 96: 5111–5116.
  • Wagner GP, Chiu C, Laubichler M. 2000. Developmental evolution as a mechanistic science: the inference from developmental mechanisms to evolutionary processes. Am Zool 40: 819–831.
  • Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100: 423–434.
  • Weishampel DB, Dodson P, Osmolska H,editors. 2004. The Dinosauria. Berkeley: University of California Press.
  • Welten MCM, Verbeek FJ, Meijer AH, Richardson MK. 2005. Gene expression and digit homology in the chicken embryo wing. Evol Dev 7: 18–28.
    Direct Link:
  • Xu X, Clark JM, Forster CA, Norell MA, Erickson GM, Eberth DA, Jia C, Zhao Q. 2006. A basal tyrannosauroid dinosaur from the late Jurassic of China. Nature 439: 715–718.
  • Xu X, Clark JM, Mo J, Choiniere J, Forster CA, Erickson GM, Hone DWE, Sullivan C, Eberth DA, Nesbitt S, Zhao Q, Hernandez R, Jia C-k, Han F-l, Guo Y. 2009. A Jurassic ceratosaur from China helps clarify avian digital homologies. Nature 459: 940–944.
  • Yang J, Lusk R, Li WH. 2003. Organismal complexity, protein complexity, and gene duplicability. Proc Natl Acad Sci U S A 100: 15661–15665.
  • Young RL, Wagner GP. 2010. Examining the mechanistic basis of the digit identity frame shift in birds. In: 11th International Conference on Limb Development and Regeneration. Williamsburg, VA.
  • Young RL, Wagner GP. 2011. Why ontogenetic homology criteria can be misleading: lessons from digit identity transformations. J Exp Zool Mol Dev Evol [DOI: 10.1002/jez.b.21396].
  • Young RL, Caputo V, Giovannotti M, Kohlsdorf T, Vargas AO, May GE, Wagner GP. 2009. Evolution of digit identity in the three-toed Italian skink Chalcides chalcides: a new case of digit identity frame shift. Evol Dev 11: 647–658.
    Direct Link:
  • Zheng X-T, You H-L, Xing X, Dong Z-M. 2009. An early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature 458: 333–336.
View Full Article (HTML) Get PDF (449K)