Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 807

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Fossils, genes and the evolution of animal limbs

Shubin, Neil, Tabin, Cliff, Carroll, Sean·1997·Nature

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/41710

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 3 references

Research works printed but not linked: 112

  1. Müller, G. B. & Wagner, G. P. Novelty in evolution: Restructuring the concept. Ann. Rev. Ecol. Syst. 22, 229–256 (1991). · doi:10.1146/annurev.es.22.110191.001305 · Paper page
  2. Coates, M. I. The origin of vertebrate limbs. Development (suppl.) 169–180 (1994). · DOI · Paper page
  3. Coates, M. I. Fish fins or tetrapod limbs—a simple twist of fate? Curr. Biol. 5, 844–848 (1995). · DOI
  4. Shubin, N. The evolution of paired fins and the origin of tetrapod limbs. Evol. Biol. 28, 39–85 (1995). · DOI
  5. Johnson, R. & Tabin, C. The long and short of hedgehog signaling. Cell 81, 313–316 (1995). · DOI
  6. Nelson, C. E. et al. Analysis of Hox gene expression in the chick limb bud. Development 122, 1449–1466 (1996). · DOI · Paper page
  7. Tabin, C. J. & Laufer, E. Hox genes and serial homology. Nature 361, 692–693 (1993). · DOI
  8. 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). · DOI · Paper page
  9. Kessel, M. & Gruss, P. Murine developmental control genes. Science 249, 374–379 (1990). · DOI · Paper page
  10. 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).
  11. 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). · DOI
  12. 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). · DOI · Paper page
  13. 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). · DOI · Paper page
  14. Vorobyeva, E. & Hinchliffe, J. R. From fins to limbs. Evol. Biol. 29, 263–311 (1996).
  15. Hinchliffe, J. R. & Johnson, D. R. The Development of the Vertebrate Limb (Clarendon, Oxford, 1980).
  16. Holmgren, N. On the origin of the tetrapod limb. Acta Zoologica 14, 185–295 (1933). · DOI · Paper page
  17. Holmgren, N. Contribution on the question of the origin of the tetrapod limb. Acta Zoologica 20, 89–124 (1939). · DOI
  18. Watson, D. M. S. On the primitive tetrapod limb. Anat. Anzeiger 44, 24–27 (1913).
  19. 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). · DOI
  20. Sordino, P. & Duboule, D. Amolecular approach to the evolution of vertebrate paired appendages. Trends Ecol. Evol. 11, 114–119 (1996). · DOI
  21. Ahlberg, P. E. & Milner, A. R. The origin and early diversification of tetrapods. Nature 368, 507–512 (1994). · DOI · Paper page
  22. Yokouchi, Y. et al. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353, 443–445 (1991). · DOI · Paper page
  23. 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).
  24. 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). · DOI
  25. 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). · DOI · Paper page
  26. Shubin, N. & Alberch, P. Amorphogenetic approach to the origin and basic organization of the tetrapod limb. Evol. Biol. 20, 318–390 (1986).
  27. Tabin, C. J. Why we have (only) five fingers per hand: hox genes and the evolution of paired limbs. Development 116, 289–296 (1992). · DOI · Paper page
  28. Holder, N. Developmental constraints and the evolution of vertebrate digit patterns. J. Theor. Biol. 104, 451–471 (1983). · DOI
  29. Morse, E. On the tarsus and carpus of birds. Ann. Lyc. Nat. Hist. 10, 141–158 (1872). · doi:10.1080/00222937208696661
  30. 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). · DOI
  31. 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). · DOI
  32. Lande, R. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32, 73–92 (1978). · DOI · Paper page
  33. Gauthier, J. Saurischian monophyly and the origin of birds. Mem. Calif. Acad. Sci. 8, 1–55 (1986).
  34. MacFadden, B. J. Fossil Horses (Cambridge Univ. Press, 1992).
  35. 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). · DOI · Paper page
  36. 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). · DOI · Paper page
  37. 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). · DOI
  38. Dollé, P. et al. Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell 75, 431–441 (1993). · DOI · Paper page
  39. 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). · DOI
  40. Capecchi, M. R. Function of homeobox genes in skeletal development. Ann. N. Y. Acad. Sci. 97, 34–37 (1996). · doi:10.1111/j.1749-6632.1996.tb56241.x
  41. Wigglesworth, V. B. Evolution of insect wings and flight. Nature 246, 127–203 (1973). · DOI
  42. Budd, G. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29, 1–14 (1996). · DOI · Paper page
  43. Hou, X. G. & Bergström, J. Cambrian lobopodians—ancestors of extant onychophorans? Zool. J. Linn. Soc. Lond. 114, 3–19 (1995). · DOI
  44. 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).
  45. Budd, G. ACambrian gilled lobopod from Greenland. Nature 364, 709–711 (1993). · DOI
  46. Chen, J. Y., Ramsköld, L. & Zhou, G. Q. Evidence for monophyly and arthropod affinity of Cambrian giant predators. Science 264, 1304–1308 (1994). · DOI · Paper page
  47. Carroll, S. B. Homeotic genes and the evolution of arthropods and chordates Nature 376, 479–485 (1995). · DOI · Paper page
  48. Struhl, G. Genes controlling segmental specification in the Drosophila thorax. Proc. Natl Acad. Sci. USA 79, 7380–7384 (1982). · DOI · Paper page
  49. Struhl, G. Ahomoeotic mutation transforming leg to antenna in Drosophila. Nature 292, 635–638 (1981). · DOI · Paper page
  50. Gibson, G. & Gehring, W. J. Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development. Development 102, 657–675 (1988). · DOI
  51. Stuart, J., Brown, S., Beeman, R. & Denell, R. Adeficiency of the homeotic complex of the beetle Tribolium. Nature 350, 72–47 (1991). · DOI · Paper page
  52. Averof, M. & Akam, M. Hox genes and the diversification of insect–crustacean body plans. Nature 376, 420–423 (1995). · DOI · Paper page
  53. 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). · DOI · Paper page
  54. Panganiban, G. et al. The development of crustacean limbs and the evolution of arthropods. Science 270, 1363–1366 (1995). · DOI · Paper page
  55. Manton, S. M. Mandibular Mechanisms and the Evolution of Arthropods Vol. 247 (British Museum and Queen Mary College, London, 1964).
  56. Wheeler, W. C., Cartwright, P. & Hayashi, C. Y. Arthropod phylogeny: a combined approach. Cladistics 9, 1–39 (1993). · DOI · Paper page
  57. 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). · DOI · Paper page
  58. 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). · DOI · Paper page
  59. Cohen, S. et al. Distal-less encodes a homeodomain protein required for limb development in Drosophila. Nature 338, 432–434 (1989). · DOI · Paper page
  60. Panganiban, G., Nagy, L. & Carroll, S. B. The development and evolution of insect limb types. Curr. Biol. 4, 671–675 (1994). · DOI · Paper page
  61. Popadic, A., Rusch, D., Peterson, M., Rogers, B. T. & Kaufman, T. C. Origin of the arthropod mandible. Nature 380, 395 (1996). · DOI
  62. Jeram, A. J., Selden, P. A. & Edwards, D. Land animals in the Silurian: Arachinids and myriapods from Shropshire, England. Science 250, 658–661 (1990). · DOI · Paper page
  63. Kukalová-Peck, J. The Insects of Australia 2nd edn (Cornell University Press, Ithaca, NY, 1991).
  64. Snodgrass, R. Principles of Insect Morphology (McGraw-Hill, New York, 1935).
  65. . 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). · DOI · Paper page
  66. Marden, J. H. & Kramer, M. G. Surface-skimming stoneflies: A possible intermediate stage in insect flight evolution. Science 266, 427–430 (1994). · DOI
  67. 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). · DOI · Paper page
  68. Carroll, S. B. et al. Pattern formation and eyespot determination in butterfly wings. Science 265, 109–114 (1994). · DOI · Paper page
  69. Averof, M. & Cohen, S. M. Evolutionary origin of insect wings from ancestral gills. Nature 385, 627–630 (1997). · DOI · Paper page
  70. 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). · DOI · Paper page
  71. Basler, D. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214 (1994). · DOI · Paper page
  72. 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). · DOI · Paper page
  73. Capdevila, J. & Guerrero, I. The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 6, 715–729 (1994).
  74. 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). · DOI
  75. Nellen, D., Burke, R., Struhl, G. & Basler, K. Direct and long-range actions of a Dpp morphogen gradient. Cell 85, 357–368 (1996). · DOI · Paper page
  76. Lecuit, T. et al. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 387–393 (1996). · DOI · Paper page
  77. 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). · DOI · Paper page
  78. 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). · DOI · Paper page
  79. Chang, D. T. et al. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120, 3339–3353 (1994). · DOI · Paper page
  80. Riddle, R. D. et al. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416 (1995). · DOI · Paper page
  81. Tickle, C. Genetics and limb development. Dev. Genet. 19, 1–8 (1996). · doi:10.1002/(sici)1520-6408(1996)19:1<1::aid-dvg1>3.0.co;2-d
  82. 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). · DOI · Paper page
  83. 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). · doi:10.1242/dev.120.3.535
  84. 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). · DOI · Paper page
  85. 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). · doi:10.1016/s0960-9822(95)00281-8
  86. 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). · DOI · Paper page
  87. Kim, J. et al. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382, 133–138 (1996). · DOI · Paper page
  88. 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).
  89. 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). · DOI · Paper page
  90. Laufer, E. et al. Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386, 366–373 (1997). · DOI · Paper page
  91. 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). · DOI · Paper page
  92. Couso, J. P., Bate, M. & Martinez-Ariias, A. Awingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259, 484–489 (1993). · DOI · Paper page
  93. 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). · DOI · Paper page
  94. 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). · DOI · Paper page
  95. Vogel, A. et al. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716–720 (1995). · DOI · Paper page
  96. Raff, R. The Shape of Life (Univ. Chicago Press, 1996). · DOI · Paper page
  97. Panganiban, G. et al. The origin and evolution of animal appendages. Proc. Natl Acad. Sci. USA 94, 5162–5166 (1997). · DOI · Paper page
  98. 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). · DOI
  99. 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). · DOI · Paper page
  100. Roth, V. L. Homology and hierarchies: Problems solved and unresolved. J. Evol. Biol. 4, 167–194 (1991). · DOI
  101. Wagner, G. P. The origin of morphological characters and the biological basis of homology. Evolution 43, 1157–1171 (1989). · DOI · Paper page
  102. Bolker, J. A. & Raff, R. A. Developmental genetics and traditional homology. BioEssays 18, 489–494 (1996). · DOI · Paper page
  103. Carroll, R. L. Vertebrate Paleontology (Freeman, San Francisco, 1988).
  104. Jarvik, E. The Structure and Evolution of the Vertebrates Vol. 1 (Academic, New York, 1980).
  105. Jarvik, E. The Devonian tetrapod Ichthyostega. Fossils and Strata 40, 1–213 (1996). · DOI
  106. 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). · DOI · Paper page
  107. 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). · DOI
  108. Mortlock, D. P. & Innis, J. W. Mutation of HOXA13 in hand–foot–genital syndrome. Nature Genet. 15, 179–181 (1997). · DOI · Paper page
  109. 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). · DOI · Paper page
  110. Summerbell, D., Lewis, J. H. & Wolpert, L. Postional information in chick limb morphogenesis. Nature 244, 492–496 (1973). · DOI · Paper page
  111. Lebedev, O. A. & Coates, M. I. The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev. Zool. J. Linn. Soc. 113, 302–348 (1995).
  112. 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).

Cited by

See all 807

Metadata

Authors
Shubin, N., Tabin, C., & Carroll, S.
Venue
Nature
Published
1997-08-14
Volume
388
Issue
6643
Pages
639-648
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W1601043516
Cited by
807
References
3
FWCI
13.84
Type
journal article
Language
en
Open access
closed
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Fossils, genes and the evolution of animal limbs. https://app.cochat.ai/papers/10.1038/41710
The paper
Shubin, N., Tabin, C., & Carroll, S. (1997). Fossils, genes and the evolution of animal limbs. Nature. https://doi.org/10.1038/41710

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.