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An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish

Nature volume 447, pages 473–476 (2007)Cite this article

Abstract

Comparative analyses of Hox gene expression and regulation in teleost fish and tetrapods support the long-entrenched notion that the distal region of tetrapod limbs, containing the wrist, ankle and digits, is an evolutionary novelty1,2,3,4. Data from fossils support the notion that the unique features of tetrapod limbs were assembled over evolutionary time in the paired fins of fish5. The challenge in linking developmental and palaeontological approaches has been that developmental data for fins and limbs compare only highly derived teleosts and tetrapods; what is lacking are data from extant taxa that retain greater portions of the fin skeletal morphology considered primitive to all bony fish6,7. Here, we report on the expression and function of genes implicated in the origin of the autopod in a basal actinopterygian, Polyodon spathula. Polyodon exhibits a late-phase, inverted collinear expression of 5′ HoxD genes, a pattern of expression long considered a developmental hallmark of the autopod and shown in tetrapods to be controlled by a ‘digit enhancer’ region. These data show that aspects of the development of the autopod are primitive to tetrapods and that the origin of digits entailed the redeployment of ancient patterns of gene activity.

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Figure 1: Expression of Shh pathway genes in Polyodon pectoral fins by stage.
Figure 2: Expression of HoxA genes in Polyodon pectoral fins.
Figure 3: Expression of HoxD genes in the pectoral fin of Polyodon.
Figure 4: Conservation of late-phase HoxD expression in bony fish (osteichthyes).

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Acknowledgements

We thank the Kahrs family and Osage Catfisheries for their continuing support of our research. This project is dedicated to the memory of John and Jim Kahrs, without whom Polyodon would not have been available for this research. M.C.D is supported by the University of Chicago, N.H.S. is supported by grants from the University of Chicago, the NSF and the NIH (NRSA to R.D.D.).

Sequences for Polyodon Shh, Ptc1, dHAND, Gli3, Hoxa11, Hoxa13, Hoxd11, Hoxd12, and Hoxd13 are deposited in Genbank with accession numbers: Shh (1,006 bp, EF100659), Ptc1 (1,253 bp, EF527815), dHAND (278 bp, EF527816), Gli3 (1,045 bp, EF534083), Hoxd11 (486 bp, EF527819), Hoxd12 (420 bp, EF527820), and Hoxd13 (863 bp, EF527821), Hoxa11 (660 bp, EF527817), Hoxa13 (833 bp, EF52718).

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Authors and Affiliations

  1. Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, Illinois 60637, USA,

    Marcus C. Davis, Randall D. Dahn & Neil H. Shubin

  2. Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA,

    Neil H. Shubin

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  1. Marcus C. Davis
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Correspondence to Neil H. Shubin.

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Davis, M., Dahn, R. & Shubin, N. An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature 447, 473–476 (2007). https://doi.org/10.1038/nature05838

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