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Evidence that mechanisms of fin development evolved in the midline of early vertebrates

Abstract

The origin of paired appendages was a major evolutionary innovation for vertebrates, marking the first step towards fin- (and later limb-) driven locomotion. The earliest vertebrate fossils lack paired fins but have well-developed median fins1,2, suggesting that the mechanisms of fin development were assembled first in the midline. Here we show that shark median fin development involves the same genetic programs that operate in paired appendages. Using molecular markers for different cell types, we show that median fins arise predominantly from somitic (paraxial) mesoderm, whereas paired appendages develop from lateral plate mesoderm. Expression of Hoxd and Tbx18 genes, which specify paired limb positions3,4, also delineates the positions of median fins. Proximodistal development of median fins occurs beneath an apical ectodermal ridge, the structure that controls outgrowth of paired appendages5,6,7. Each median fin bud then acquires an anteroposteriorly-nested pattern of Hoxd expression similar to that which establishes skeletal polarity in limbs8,9. Thus, despite their different embryonic origins, paired and median fins utilize a common suite of developmental mechanisms. We extended our analysis to lampreys, which diverged from the lineage leading to gnathostomes before the origin of paired appendages2,10, and show that their median fins also develop from somites and express orthologous Hox and Tbx genes. Together these results suggest that the molecular mechanisms for fin development originated in somitic mesoderm of early vertebrates, and that the origin of paired appendages was associated with re-deployment of these mechanisms to lateral plate mesoderm.

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Acknowledgements

We thank A. Burke, P. Mabee, P. Crotwell and B. Shockey for commenting on the manuscript, A. Graham for sharing reagents, and L. Page and G. Weddle for assistance with lamprey collection. R. Freitas is a PhD student of the GABBA Program (ICBAS, Univ. Oporto) and was supported by a fellowship from FCT, Praxis XXI. Author contributions R.F. performed and designed (with M.J.C.) the reported studies. G.Z. performed part of the gene cloning and phylogenetic analyses. M.J.C. supervised the research project, and assisted in the experimental design. R.F. and M.J.C. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Martin J. Cohn.

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Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. Sequences for Foxc2, Zic1, Scleraxis, Pax7, Hoxd9, Hoxd10, Hoxd12, Hoxd13 and Tbx18 from S. canicula, and Parascleraxis and Tbx15/18 from P. marinus, are deposited in GenBank under accession numbers DQ659101–DQ659111. The authors declare no competing financial interests.

Additional information

Sequences for Foxc2, Zic1, Scleraxis, Pax7, Hoxd9, Hoxd10, Hoxd12, Hoxd13 and Tbx18 from S. canicula, and Parascleraxis and Tbx15/18 from P. marinus, are deposited in GenBank under accession numbers DQ659101–DQ659111.

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Supplementary Notes

This file contains Supplementary Figures 1–8, Supplementary Methods, and seven references. (PDF 13253 kb)

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Further reading

Figure 1: Developmental origin of catshark median fins.
Figure 2: Regionalized expression of Hoxd genes and Tbx18 along the median finfold of catsharks.
Figure 3: Anteroposterior nesting of Hoxd gene expression in catshark median fin buds.
Figure 4: Lamprey median fin development.

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