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Fin development in a cartilaginous fish and the origin of vertebrate limbs

Abstract

Recent fossil finds and experimental analysis of chick and mouse embryos highlighted the lateral fin fold theory, which suggests that two pairs of limbs in tetrapods evolved by subdivision of an elongated single fin1. Here we examine fin development in embryos of the primitive cartilaginous fish, Scyliorhinus canicula (dogfish) using scanning electron microscopy and investigate expression of genes known to be involved in limb positioning, identity and patterning in higher vertebrates. Although we did not detect lateral fin folds in dogfish embryos, Engrailed-1 expression suggests that the body is compartmentalized dorso-ventrally. Furthermore, specification of limb identity occurs through the Tbx4 and Tbx5 genes, as in higher vertebrates. In contrast, unlike higher vertebrates, we did not detect Shh transcripts in dogfish fin-buds, although dHand (a gene involved in establishing Shh) is expressed. In S. canicula, the main fin axis seems to lie parallel to the body axis. ‘Freeing’ fins from the body axis and establishing a separate ‘limb’ axis has been proposed to be a crucial step in evolution of tetrapod limbs2,3. We suggest that Shh plays a critical role in this process.

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Figure 1: Scanning electron micrographs of S. canicula embryos.
Figure 2: Model for evolution of vertebrate paired appendages.
Figure 3: Gene expression patterns of stage 27–28 S. canicula embryos.
Figure 4: A, Series of pectoral appendages comparing the dogfish with other species in which the metapterygial axis is freed from the body wall and forms the main axis of the limb.

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References

  1. Thacher, J. K. Median and paired fins, a contribution to the history of vertebrate limbs. Trans. Conn. Acad. 3, 281–310 (1877).

    Google Scholar 

  2. Jarvik, E. in Basic Structure and Evolution of Vertebrates 109–131 (Academic, London, 1980).

    Google Scholar 

  3. Moy-Thomas, J. A. The evolution of the pectoral fins of fishes and the tetrapod forelimb. School Sci. Rev. 36, 592–599 (1936).

    Article  Google Scholar 

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

  5. Shu, D.-G. et al. Lower Cambrian vertebrates from South China. Nature 402, 42–46 (1999).

    Article  ADS  CAS  Google Scholar 

  6. Neyt, C. et al. Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82–86 (2000).

    Article  ADS  CAS  Google Scholar 

  7. Balfour, F. M. The development of elasmobranch fishes. J. Anat. Physiol. Lond. 11, 128–172 (1876).

    CAS  Google Scholar 

  8. Ballard, W. W., Mellinger, J. & Lechenault, H. A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliohinidae). J. Exp. Zool. 267, 318–336 (1993).

    Article  Google Scholar 

  9. Altabef, M., Clarke, J. D. & Tickle, C. Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124, 4547–4556 (1997).

    CAS  PubMed  Google Scholar 

  10. Tanaka, M. et al. Apical ectodermal ridge induction by the transplantation of En-1-overexpressing ectoderm in chick limb bud. Dev. Growth Differ. 40, 423–429 (1998).

    Article  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

  12. Coates, M. I. Hox genes, fin folds and symmetry. Nature 364, 195–196 (1993).

    Article  ADS  Google Scholar 

  13. Tamura, K. et al. Evolutionary aspects of positioning and identification of vertebrate limbs. J. Anat. 199, 195–204 (2001).

    Article  CAS  Google Scholar 

  14. Ruvinsky, I., Silver, L. M. & Gibson-Brown, J. J. Phylogenetic analysis of T-box genes demonstrates the importance of amphioxus for understanding evolution of the vertebrate genome. Genetics 156, 1249–1257 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Balinsky, B. I. Das extremitaetenseitenfeld, seine ausdehnung und beschaffenheit. Roux Arch. Dev. Biol 130, 704–736 (1933).

    Article  CAS  Google Scholar 

  16. Cohn, M. J., Izpisua-Belmonte, J. C., Abud, H., Heath, J. K. & Tickle, C. Fibroblast growth factors induce additional limb development from the flank of chick embryo. Cell 80, 739–746 (1995).

    Article  CAS  Google Scholar 

  17. Tanaka, M. et al. Distribution of polarizing activity and potential for limb formation in mouse and chick embryos and possible relationship to polydactyly. Development 127, 4011–4021 (2000).

    CAS  PubMed  Google Scholar 

  18. Riddle, R. D., Johnson, R. L., Laufer, E. & Tabin, C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416 (1993).

    Article  CAS  Google Scholar 

  19. Ekker, S. C. et al. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr. Biol. 5, 44–55 (1995).

    Article  Google Scholar 

  20. Cohn, M. J. Giving limbs a hand. Nature 406, 953–954 (2000).

    Article  CAS  Google Scholar 

  21. Tümpel, S. et al. Antero-posterior signaling in vertebrate limb development and stripes of Tbx3 expression. Dev. Biol (submitted).

  22. Kraus, P., Fraidenraich, D. & Loomis, C. A. Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech. Dev. 100, 45–58 (2001).

    Article  CAS  Google Scholar 

  23. Mazan, S., Jaillard, D., Baratte, B. & Janvier, P. Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol. Dev. 2, 186–193 (2000).

    Article  CAS  Google Scholar 

  24. Wilkinson, D. G. In Situ Hybridization: A Practical Approach 75–83 (IRL Press/Oxford Univ. Press, Oxford, 1992).

    Google Scholar 

  25. Kuratani, S., Ueki, T., Aizawa, S. & Hirano, S. Peripheral development of cranial nerves in a cyclostome, Lampetra japonica: morphological distribution of nerve branches and the vertebrate body plan. J. Comp. Neurol. 384, 482–500 (1997).

    Article  Google Scholar 

  26. Schlosser, G. & Roth, G. Evolution of nerve development in frogs. I. The development of the peripheral nervous system in Discoglossus pictus (Discoglossidae). Brain Behav. Evol. 50, 61–93 (1997).

    Article  CAS  Google Scholar 

  27. Münsterberg, A. E., Kitajewski, J., Bumcrot, D. A., McMahon, A. P. & Lassar, A. B. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911–2922 (1995).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to A. Wells for his assistance in maintenance of S. canicula embryos, S. Kuratani for information about S. canicula developmental studies before publication, S. Mazan for technical advice and ScOtx1and ScOtx2 cDNA as positive control probes for establishing in situ hybridization methods and N. Helps for DNA sequencing. M.T. is supported by JSPS Postdoctoral Fellowships for Research Abroad, JSPS Research Fellowships for Young Scientists and the Inoue Research Award for Young Scientists. A.M. is supported by a Wellcome Trust research Career Development Award. C.T. is Foulerton Research Professor of The Royal Society.

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Tanaka, M., Münsterberg, A., Anderson, W. et al. Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 416, 527–531 (2002). https://doi.org/10.1038/416527a

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