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Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning

Abstract

The genetic mechanisms regulating tetrapod limb development are well characterized, but how they were assembled during evolution and their function in basal vertebrates is poorly understood. Initial studies report that chondrichthyans, the most primitive extant vertebrates with paired appendages, differ from ray-finned fish and tetrapods in having Sonic hedgehog (Shh)-independent patterning of the appendage skeleton1. Here we demonstrate that chondrichthyans share patterns of appendage Shh expression, Shh appendage-specific regulatory DNA, and Shh function with ray-finned fish and tetrapods2,3,4,5,6,7,8,9,10. These studies demonstrate that some aspects of Shh function are deeply conserved in vertebrate phylogeny, but also highlight how the evolution of Shh regulation may underlie major morphological changes during appendage evolution.

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Figure 1: Shh is expressed in wild-type and retinoic acid (RA)-treated basal vertebrate appendages.
Figure 2: Retinoic acid effects dose- and stage-dependent fin skeleton alterations in chondrichthyans.
Figure 3: Retinoic acid induces ectopic elements and posteriorizes skate fin structures.

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Acknowledgements

We thank A. Tullis of The University of Puget Sound, Marine Biological Laboratories at Woods Hole, K. Riley of Chicago Aquarium and Pond for specimens, K. Tamura and T. Sagai for sharing unpublished data, P. Beachy for assistance, and K. Monoyios for illustration and graphics assistance. This work was supported by fellowships from The National Institutes of Health (R.D.D.), The Jane Coffin Childs Memorial Fund for Medical Research (W.N.P.), and the Division of Biological Sciences at The University of Chicago (N.H.S.).

Author Contributions All experiments were designed and data generated by R.D.D., except for isolation of full-length skate Shh cDNA (W.N.P.) and the Polyodon data (M.C.D.). Data were analysed and the manuscript prepared by R.D.D. and N.H.S.

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Correspondence to Neil H. Shubin.

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Dahn, R., Davis, M., Pappano, W. et al. Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature 445, 311–314 (2007). https://doi.org/10.1038/nature05436

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