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

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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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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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  1. Andrea Münsterberg

    Present address: School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

Authors and Affiliations

  1. Division of Cell and Developmental Biology, Wellcome Trust Biocentre, University of Dundee, Dow Street, Dundee, DD1 5EH, UK

    Mikiko Tanaka, Andrea Münsterberg & Cheryll Tickle

  2. Division of Cell Biology and Immunology, Wellcome Trust Biocentre, University of Dundee, Dow Street, Dundee, DD1 5EH, UK

    Alan R. Prescott

  3. School of Biology, Division of Environmental and Evolutionary Biology, Gatty Marine Lab, University of St Andrews, St Andrews, KY16 8LB, Fife, UK

    W. Gary Anderson & Neil Hazon

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  1. Mikiko Tanaka
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  2. Andrea Münsterberg
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Correspondence to Mikiko Tanaka.

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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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