Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Fossils, genes and the evolution of animal limbs

Abstract

The morphological and functional evolution of appendages has played a crucial role in the adaptive radiation of tetrapods, arthropods and winged insects. The origin and diversification of fins, wings and other structures, long a focus of palaeontology, can now be approached through developmental genetics. Modifications of appendage number and architecture in each phylum are correlated with regulatory changes in specific patterning genes. Although their respective evolutionary histories are unique, vertebrate, insect and other animal appendages are organized by a similar genetic regulatory system that may have been established in a common ancestor.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Major innovations of vertebrate paired appendages.
Figure 2: Stylopod, zeugopod, and autopod: patterning the limb.
Figure 3: The origin of digits.
Figure 4: The lobopod–arthropod transition and the diversification of arthropod limb patterns.
Figure 5: The evolution of the arthropod limb and the origin of the insect wing.
Figure 6: A cladogram of selected metazoans shows the distribution of major genes involved with appendage development.

Similar content being viewed by others

References

  1. Müller, G. B. & Wagner, G. P. Novelty in evolution: Restructuring the concept. Ann. Rev. Ecol. Syst. 22, 229–256 (1991).

    Article  Google Scholar 

  2. Coates, M. I. The origin of vertebrate limbs. Development (suppl.) 169–180 (1994).

  3. Coates, M. I. Fish fins or tetrapod limbs—a simple twist of fate? Curr. Biol. 5, 844–848 (1995).

    Article  CAS  PubMed  Google Scholar 

  4. Shubin, N. The evolution of paired fins and the origin of tetrapod limbs. Evol. Biol. 28, 39–85 (1995).

    Article  Google Scholar 

  5. Coates, M. I. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution. Trans. R. Soc. Edinb. 87, 363–421 (1996).

    Article  Google Scholar 

  6. Johnson, R. & Tabin, C. The long and short of hedgehog signaling. Cell 81, 313–316 (1995).

    Article  CAS  PubMed  Google Scholar 

  7. Nelson, C. E. et al. Analysis of Hox gene expression in the chick limb bud. Development 122, 1449–1466 (1996).

    CAS  PubMed  Google Scholar 

  8. Tabin, C. J. & Laufer, E. Hox genes and serial homology. Nature 361, 692–693 (1993).

    Article  ADS  Google Scholar 

  9. Sordino, P., van der Hoeven, F. & Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Kessel, M. & Gruss, P. Murine developmental control genes. Science 249, 374–379 (1990).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Mackem, S., Ranson, M. & Mahon, K. Limb-type differences in expression domains of certain chick Hox-4 genes and relationship to pattern modification for flight. Prog. Clin. Biol. Res. 383 A, 21–30 (1993).

    Google Scholar 

  12. Peterson, R. J., Papenbrock, T., Davada, M. M. & Awgulewitschh, A. The murine Hoxc cluster contains five neighboring abdB-related Hox genes that show unique spatially coordinated expression in posterior embryonic subregions. Mech. Dev. 47, 253–260 (1994).

    Article  CAS  PubMed  Google Scholar 

  13. Gibson-Brown, J. J. et al. Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech. Dev. 56, 93–101 (1996).

    Article  CAS  PubMed  Google Scholar 

  14. Davis, A. P., Witte, D. P., Hsieh-Li, H. M., Potter, S. S. & Capecchi, M. R. Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 375, 791–795 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Vorobyeva, E. & Hinchliffe, J. R. From fins to limbs. Evol. Biol. 29, 263–311 (1996).

    Google Scholar 

  16. Hinchliffe, J. R. & Johnson, D. R. The Development of the Vertebrate Limb (Clarendon, Oxford, 1980).

    Google Scholar 

  17. Holmgren, N. On the origin of the tetrapod limb. Acta Zoologica 14, 185–295 (1933).

    Article  Google Scholar 

  18. Holmgren, N. Contribution on the question of the origin of the tetrapod limb. Acta Zoologica 20, 89–124 (1939).

    Article  Google Scholar 

  19. Watson, D. M. S. On the primitive tetrapod limb. Anat. Anzeiger 44, 24–27 (1913).

    Google Scholar 

  20. Gregory, W. K. & Raven, H. C. Studies on the origin and early evolution of paired fins and limbs. Ann. N. Y. Acad. Sci. 42, 273–360 (1941).

    Article  ADS  Google Scholar 

  21. Sordino, P. & Duboule, D. Amolecular approach to the evolution of vertebrate paired appendages. Trends Ecol. Evol. 11, 114–119 (1996).

    Article  CAS  PubMed  Google Scholar 

  22. Ahlberg, P. E. & Milner, A. R. The origin and early diversification of tetrapods. Nature 368, 507–512 (1994).

    Article  ADS  Google Scholar 

  23. Yokouchi, Y. et al. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353, 443–445 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Gerard, M., Duboule, D. & Zakany, J. C. Cooperation of regulatory elements involved in the activation of the Hoxd-11 gene. Compt. R. Acad. Sci. III 316, 985–994 (1993).

    CAS  Google Scholar 

  25. Beckers, J., Gerard, M. & Duboule, D. Transgenic analysis of a potential Hoxd-11 limb regulatory element present in tetrapods and fish. Dev. Biol. 180, 543–553 (1996).

    Article  CAS  PubMed  Google Scholar 

  26. van der Hoeven, F., Zakany, J. & Duboule, D. Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 85, 1025–1035 (1996).

    Article  CAS  PubMed  Google Scholar 

  27. Shubin, N. & Alberch, P. Amorphogenetic approach to the origin and basic organization of the tetrapod limb. Evol. Biol. 20, 318–390 (1986).

    Google Scholar 

  28. Tabin, C. J. Why we have (only) five fingers per hand: hox genes and the evolution of paired limbs. Development 116, 289–296 (1992).

    CAS  PubMed  Google Scholar 

  29. Holder, N. Developmental constraints and the evolution of vertebrate digit patterns. J. Theor. Biol. 104, 451–471 (1983).

    Article  CAS  PubMed  Google Scholar 

  30. Morse, E. On the tarsus and carpus of birds. Ann. Lyc. Nat. Hist. 10, 141–158 (1872).

    Article  Google Scholar 

  31. Shubin, N., Crawford, A. & Wake, D. Morphological variation in the limbs of Taricha granulosa (Caudata: Salamandridae): Evolutionary and phylogenetic implications. Evolution 49, 874–884 (1995).

    Article  PubMed  Google Scholar 

  32. Greer, A. 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 (1980).

    Article  Google Scholar 

  33. Lande, R. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32, 73–92 (1978).

    Article  PubMed  Google Scholar 

  34. Gauthier, J. Saurischian monophyly and the origin of birds. Mem. Calif. Acad. Sci. 8, 1–55 (1986).

    Google Scholar 

  35. MacFadden, B. J. Fossil Horses (Cambridge Univ. Press, 1992).

    Google Scholar 

  36. Davis, A. P. & Capecchi, M. R. Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11. Development 120, 2187–2198 (1994).

    CAS  PubMed  Google Scholar 

  37. Davis, A. P. & Capecchi, M. R. Amutational analysis of the 5′ HoxD genes: Dissection of genetic interactions during limb development in the mouse. Development 122, 1175–1185 (1996).

    CAS  PubMed  Google Scholar 

  38. Favier, B. et al. Functional cooperation between the non-paralogous genes Hoxa-10 and Hoxd0-11 in the developing forelimb and axial skeleton. Development 122, 449–460 (1996).

    CAS  PubMed  Google Scholar 

  39. Dollé, P. et al. Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell 75, 431–441 (1993).

    Article  PubMed  Google Scholar 

  40. Favier, B., LeMeur, M., Chambon, P. & Dollé, P. Axial skeleton homeosis and forelimb malformations in Hoxd-11 mutant mice. Proc. Natl Acad. Sci. USA 92, 310–314 (1995).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  41. Capecchi, M. R. Function of homeobox genes in skeletal development. Ann. N. Y. Acad. Sci. 97, 34–37 (1996).

    Article  ADS  Google Scholar 

  42. Wigglesworth, V. B. Evolution of insect wings and flight. Nature 246, 127–203 (1973).

    Article  ADS  Google Scholar 

  43. Budd, G. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29, 1–14 (1996).

    Article  Google Scholar 

  44. Hou, X. G. & Bergström, J. Cambrian lobopodians—ancestors of extant onychophorans? Zool. J. Linn. Soc. Lond. 114, 3–19 (1995).

    Article  Google Scholar 

  45. Simonetta, A. M. & Delle Cave, L. in The Early Evolution of Metazoa and the Significance of Problematic Taxa (eds Simonetta, A. M. & Conway Morris, S.) 189–244 (Cambridge Univ. Press, 1991).

    Google Scholar 

  46. Budd, G. ACambrian gilled lobopod from Greenland. Nature 364, 709–711 (1993).

    Article  ADS  Google Scholar 

  47. Chen, J. Y., Ramsköld, L. & Zhou, G. Q. Evidence for monophyly and arthropod affinity of Cambrian giant predators. Science 264, 1304–1308 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  48. Carroll, S. B. Homeotic genes and the evolution of arthropods and chordates Nature 376, 479–485 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Struhl, G. Genes controlling segmental specification in the Drosophila thorax. Proc. Natl Acad. Sci. USA 79, 7380–7384 (1982).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  50. Struhl, G. Ahomoeotic mutation transforming leg to antenna in Drosophila. Nature 292, 635–638 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  51. Gibson, G. & Gehring, W. J. Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development. Development 102, 657–675 (1988).

    Google Scholar 

  52. Stuart, J., Brown, S., Beeman, R. & Denell, R. Adeficiency of the homeotic complex of the beetle Tribolium. Nature 350, 72–47 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  53. Averof, M. & Akam, M. Hox genes and the diversification of insect–crustacean body plans. Nature 376, 420–423 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  54. Vachon, G. et al. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene. Cell 71, 437–450 (1992).

    Article  CAS  PubMed  Google Scholar 

  55. Panganiban, G. et al. The development of crustacean limbs and the evolution of arthropods. Science 270, 1363–1366 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  56. Manton, S. M. Mandibular Mechanisms and the Evolution of Arthropods Vol. 247 (British Museum and Queen Mary College, London, 1964).

    Google Scholar 

  57. Wheeler, W. C., Cartwright, P. & Hayashi, C. Y. Arthropod phylogeny: a combined approach. Cladistics 9, 1–39 (1993).

    Article  PubMed  Google Scholar 

  58. Boore, J. L., Collins, T. M., Stanton, D., Daehler, L. L. & Brown, W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376, 163–165 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  59. Cohen, S. M. & Jürgens, G. Proximal–distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J. 8, 2045–2055 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Cohen, S. et al. Distal-less encodes a homeodomain protein required for limb development in Drosophila. Nature 338, 432–434 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  61. Panganiban, G., Nagy, L. & Carroll, S. B. The development and evolution of insect limb types. Curr. Biol. 4, 671–675 (1994).

    Article  CAS  PubMed  Google Scholar 

  62. Popadic, A., Rusch, D., Peterson, M., Rogers, B. T. & Kaufman, T. C. Origin of the arthropod mandible. Nature 380, 395 (1996).

    Article  ADS  CAS  Google Scholar 

  63. Jeram, A. J., Selden, P. A. & Edwards, D. Land animals in the Silurian: Arachinids and myriapods from Shropshire, England. Science 250, 658–661 (1990).

    Article  ADS  CAS  PubMed  Google Scholar 

  64. Kukalová-Peck, J. The Insects of Australia 2nd edn (Cornell University Press, Ithaca, NY, 1991).

    Google Scholar 

  65. Snodgrass, R. Principles of Insect Morphology (McGraw-Hill, New York, 1935).

    Google Scholar 

  66. . Kukalova-Peck, J. Origin and evolution of insect wings and their relation to metamorphosis, as documented from the fossil record. J. Morphol. 156, 53–126 (1978).

    Article  PubMed  Google Scholar 

  67. Marden, J. H. & Kramer, M. G. Surface-skimming stoneflies: A possible intermediate stage in insect flight evolution. Science 266, 427–430 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  68. Cohen, B. et al. Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117, 597–608 (1993).

    CAS  PubMed  Google Scholar 

  69. Diaz-Benjumea, F. & Cohen, S. M. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741–752 (1993).

    Article  CAS  PubMed  Google Scholar 

  70. Carroll, S. B. et al. Pattern formation and eyespot determination in butterfly wings. Science 265, 109–114 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  71. Averof, M. & Cohen, S. M. Evolutionary origin of insect wings from ancestral gills. Nature 385, 627–630 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  72. Lee, J. J. et al. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33–50 (1992).

    Article  CAS  PubMed  Google Scholar 

  73. Tabata, T. et al. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. 6, 2635–2645 (1992).

    Article  CAS  PubMed  Google Scholar 

  74. Basler, D. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  75. Posakony, L., Raftery, L. & Gelbart, W. Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior–posterior compartment boundary. Mech. Dev. 33, 69–82 (1991).

    Article  Google Scholar 

  76. Capdevila, J. & Guerrero, I. The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 6, 715–729 (1994).

    Google Scholar 

  77. Sanicola, M., Sekelsky, J., Elson, S. & Gelbart, W. M. Drawing a stripe in Drosophila imaginal discs: negative regulation of decapentaplegic and patched expression. Genetics 139, 745–756 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Nellen, D., Burke, R., Struhl, G. & Basler, K. Direct and long-range actions of a Dpp morphogen gradient. Cell 85, 357–368 (1996).

    Article  CAS  PubMed  Google Scholar 

  79. Lecuit, T. et al. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 387–393 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  80. Echelard, Y. et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430 (1993).

    Article  CAS  PubMed  Google Scholar 

  81. Krauss, S., Concordet, J. P. & Ingham, P. W. Afunctionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444 (1993).

    Article  CAS  PubMed  Google Scholar 

  82. Chang, D. T. et al. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120, 3339–3353 (1994).

    CAS  PubMed  Google Scholar 

  83. Riddle, R. D. et al. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416 (1995).

    Article  Google Scholar 

  84. Tickle, C. Genetics and limb development. Dev. Genet. 19, 1–8 (1996).

    Article  CAS  PubMed  Google Scholar 

  85. Irvine, K. & Weischaus, E. fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79, 595–606 (1994).

    Article  CAS  PubMed  Google Scholar 

  86. Spreicher, S., Thomas, U., Hinz, U. & Knust, E. The Serrate locus of Drosophila and its role in morphogenesis or imaginal discs: control of cell proliferation. Development 120, 535–544 (1994).

    Google Scholar 

  87. Kim, J., Irvine, K. & Carroll, S. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795–802 (1995).

    Article  CAS  PubMed  Google Scholar 

  88. Couso, J. P., Knust, E. & Martinez Ariias, A. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5, 1437–1448 (1995).

    Article  CAS  PubMed  Google Scholar 

  89. Diaz-Benjumea, F. J. & Cohen, S. Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121, 4215–4225 (1995).

    CAS  PubMed  Google Scholar 

  90. Kim, J. et al. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382, 133–138 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  91. Todt, W. L. & Fallon, J. F. Development of the apical ectodermal ridge in the chick wing bud. J. Embryol. Exp. Morphol. 80, 21–41 (1984).

    CAS  PubMed  Google Scholar 

  92. Rodriguez-Estaban, C. et al. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature 386, 360–361 (1997).

    Article  ADS  Google Scholar 

  93. Laufer, E. et al. Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386, 366–373 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  94. Williams, J. A., Paddock, S. W. & Carroll, S. B. Pattern formation in a secondary field: A hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete sub-regions. Development 117, 571–584 (1993).

    CAS  PubMed  Google Scholar 

  95. Couso, J. P., Bate, M. & Martinez-Ariias, A. Awingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259, 484–489 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  96. Parr, B. A. & McMahon, A. P. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350–353 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  97. Riddle, R. D. et al. Induction of the LIM homeobox gene Lmx-1 by Wnt-7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631–640 (1995).

    Article  CAS  PubMed  Google Scholar 

  98. Vogel, A. et al. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716–720 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  99. Raff, R. The Shape of Life (Univ. Chicago Press, 1996).

    Book  MATH  Google Scholar 

  100. Panganiban, G. et al. The origin and evolution of animal appendages. Proc. Natl Acad. Sci. USA 94, 5162–5166 (1997).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  101. Wall, N. A. & Hogan, B. L. M. Expression of bone morphogenetic protein-4 (BMP-4), bone morphogenetic protein-7 (BMP-7), fibroblast growth factor-8 (FGF-8) and Sonic hedgehog (SHH) during branchial arch development in the chick. Mech. Dev. 53, 383–392 (1995).

    Article  CAS  PubMed  Google Scholar 

  102. Marigo, V., Scott, M. P., Johnson, R. L., Goodrich, L. V. & Tabin, C. J. Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122, 1225–1233 (1996).

    CAS  PubMed  Google Scholar 

  103. Roth, V. L. Homology and hierarchies: Problems solved and unresolved. J. Evol. Biol. 4, 167–194 (1991).

    Article  Google Scholar 

  104. Wagner, G. P. The origin of morphological characters and the biological basis of homology. Evolution 43, 1157–1171 (1989).

    Article  CAS  PubMed  Google Scholar 

  105. Bolker, J. A. & Raff, R. A. Developmental genetics and traditional homology. BioEssays 18, 489–494 (1996).

    Article  CAS  PubMed  Google Scholar 

  106. Carroll, R. L. Vertebrate Paleontology (Freeman, San Francisco, 1988).

    Google Scholar 

  107. Jarvik, E. The Structure and Evolution of the Vertebrates Vol. 1 (Academic, New York, 1980).

    Google Scholar 

  108. Jarvik, E. The Devonian tetrapod Ichthyostega. Fossils and Strata 40, 1–213 (1996).

    Google Scholar 

  109. Fromental-Ramain, C. et al. Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development 122, 461–472 (1996).

    CAS  PubMed  Google Scholar 

  110. Mortlock, D. P., Post, L. C. & Innis, J. W. The molecular basis of hypodactyly (Hd): a deletion in Hoxa13 leads to arrest of digital arch formation. Nature Genet. 13, 284–289 (1996).

    Article  CAS  PubMed  Google Scholar 

  111. Mortlock, D. P. & Innis, J. W. Mutation of HOXA13 in hand–foot–genital syndrome. Nature Genet. 15, 179–181 (1997).

    Article  CAS  PubMed  Google Scholar 

  112. Saunders, J. The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363–403 (1948).

    Article  PubMed  Google Scholar 

  113. Summerbell, D., Lewis, J. H. & Wolpert, L. Postional information in chick limb morphogenesis. Nature 244, 492–496 (1973).

    Article  ADS  CAS  PubMed  Google Scholar 

  114. Lebedev, O. A. & Coates, M. I. The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev. Zool. J. Linn. Soc. 113, 302–348 (1995).

    Google Scholar 

  115. Hou, X. G., Bergström, J. & Ahlberg, P. Anomalocaris and other large animals in the Lower Cambrian Chenjiang fauna of southwest China. Geol Forening. Forhandling. 117, 163–183 (1995).

    Google Scholar 

Download references

Acknowledgements

We thank P. Ahlberg, G. Budd, A. C. Burke, M. Coates, A. Meyer, G. Panganiban, P. Sniegowski, D. Wake, R. S. Winters, L. Wolpert and members of our laboratories for their critiques of drafts of this manuscript. S.B.C. is an investigator of the HHMI. C.T. is supported by grants from the NIH and the American Cancer Society. N.S. is supported by grants from the NSF, from the National Geographic Society and from the Research Foundation of the University of Pennsylvania.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Neil Shubin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shubin, N., Tabin, C. & Carroll, S. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648 (1997). https://doi.org/10.1038/41710

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/41710

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing