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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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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.

References

  1. Zhang, X. G. & Hou, X. G. Evidence for a single median fin-fold and tail in the Lower Cambrian vertebrate, Haikouichthys ercaicunensis. J. Evol. Biol. 17, 1162–1166 (2004)

    Article  Google Scholar 

  2. Coates, M. I. The origin of vertebrate limbs. Development (Suppl.), 169–182 (1994)

  3. Cohn, M. J. et al. Hox9 genes and vertebrate limb specification. Nature 387, 97–101 (1997)

    Article  ADS  CAS  Google Scholar 

  4. Tanaka, M. & Tickle, C. Tbx18 and boundary formation in chick somite and wing development. Dev. Biol. 268, 470–480 (2004)

    Article  CAS  Google Scholar 

  5. Saunders, J. W. The proximo-distal sequence of origin of parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363–403 (1948)

    Article  Google Scholar 

  6. Grandel, H. & Schulte-Merker, S. The development of the paired fins in the zebrafish (Danio rerio). Mech. Dev. 79, 99–120 (1998)

    Article  CAS  Google Scholar 

  7. Grandel, H., Draper, B. W. & Schulte-Merker, S. dackel acts in the ectoderm of the zebrafish pectoral fin bud to maintain AER signaling. Development 127, 4169–4178 (2000)

    CAS  PubMed  Google Scholar 

  8. Zakany, J., Kmita, M. & Duboule, D. A dual role for Hox genes in limb anterior-posterior asymmetry. Science 304, 1669–1672 (2004)

    Article  ADS  CAS  Google Scholar 

  9. Tarchini, B. & Duboule, D. Control of Hoxd genes collinearity during early limb development. Dev. Cell 10, 93–103 (2006)

    Article  CAS  Google Scholar 

  10. Donoghue, P. C. J., Forey, P. L. & Aldridge, R. J. Conodont affinity and chordate phylogeny. Biol. Rev. Camb. Philos. Soc. 75, 191–251 (2000)

    Article  CAS  Google Scholar 

  11. Sun, X., Mariani, F. V. & Martin, G. R. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418, 501–508 (2002)

    Article  ADS  CAS  Google Scholar 

  12. Tucker, A. S. & Slack, J. M. Independent induction and formation of the dorsal and ventral fins in Xenopus laevis. Dev. Dyn. 230, 461–467 (2004)

    Article  CAS  Google Scholar 

  13. Smith, M., Hickman, A., Amanze, D., Lumsden, A. & Thorogood, P. Trunk neural crest origin of caudal fin mesenchyme in the zebrafish Brachydanio rerio. Proc. R. Soc. Lond. B 256, 137–145 (1994)

    Article  ADS  Google Scholar 

  14. Sobkow, L., Epperlein, H. H., Herklotz, S., Straube, W. L. & Tanaka, E. M. A germline GFP transgenic axolotl and its use to track cell fate: dual origin of the fin mesenchyme during development and the fate of blood cells during regeneration. Dev. Biol. 290, 386–397 (2006)

    Article  CAS  Google Scholar 

  15. Furumoto, T. A. et al. Notochord-dependent expression of MFH1 and PAX1 cooperates to maintain the proliferation of sclerotome cells during the vertebral column development. Dev. Biol. 210, 15–29 (1999)

    Article  CAS  Google Scholar 

  16. Sun Rhodes, L. S. & Merzdorf, C. S. The zic1 gene is expressed in chick somites but not in migratory neural crest. Gene Expr. Patterns 6, 539–545 (2006)

    Article  Google Scholar 

  17. Brent, A. E., Schweitzer, R. & Tabin, C. J. A somitic compartment of tendon progenitors. Cell 113, 235–248 (2003)

    Article  CAS  Google Scholar 

  18. Brent, A. E. & Tabin, C. J. FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 131, 3885–3896 (2004)

    Article  CAS  Google Scholar 

  19. Lacosta, A. M., Muniesa, P., Ruberte, J., Sarasa, M. & Dominguez, L. Novel expression patterns of Pax3/Pax7 in early trunk neural crest and its melanocyte and non-melanocyte lineages in amniote embryos. Pigment Cell Res. 18, 243–251 (2005)

    Article  CAS  Google Scholar 

  20. Trevarrow, B., Marks, D. L. & Kimmel, C. B. Organization of hindbrain segments in the zebrafish embryo. Neuron 4, 669–679 (1990)

    Article  CAS  Google Scholar 

  21. Mabee, P. M., Crotwell, P. L., Bird, N. C. & Burke, A. C. Evolution of median fin modules in the axial skeleton of fishes. J. Exp. Zool. 294, 77–90 (2002)

    Article  Google Scholar 

  22. Sordino, P., Van der Hoeven, F. & Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995)

    Article  ADS  CAS  Google Scholar 

  23. Nelson, C. E. et al. Analysis of Hox gene expression in the chick limb bud. Development 122, 1449–1466 (1996)

    CAS  Google Scholar 

  24. Richardson, M. K. & Wright, G. M. Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus). J. Morphol. 257, 348–363 (2003)

    Article  Google Scholar 

  25. Hirata, M., Ito, K. & Tsuneki, K. Migration and colonization patterns of HNK-1-immunoreactive neural crest cells in lamprey and swordtail embryos. Zool. Sci 14, 305–312 (1997)

    Article  Google Scholar 

  26. McCauley, D. W. & Bronner-Fraser, M. Neural crest contributions to the lamprey head. Development 130, 2317–2327 (2003)

    Article  CAS  Google Scholar 

  27. Force, A., Amores, A. & Postlethwait, J. H. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J. Exp. Zool. 294, 30–46 (2002)

    Article  CAS  Google Scholar 

  28. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. & Westerfield, M. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475–3486 (1994)

    Article  CAS  Google Scholar 

  29. Akimenko, M. A., Johnson, S. L., Westerfield, M. & Ekker, M. Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development 121, 347–357 (1995)

    CAS  PubMed  Google Scholar 

  30. Freitas, R. & Cohn, M. J. Analysis of EphA4 in the lesser spotted catshark identifies a primitive gnathostome expression pattern and reveals co-option during evolution of shark-specific morphology. Dev. Genes Evol. 214, 466–472 (2004)

    Article  CAS  Google Scholar 

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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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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.

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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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Freitas, R., Zhang, G. & Cohn, M. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442, 1033–1037 (2006). https://doi.org/10.1038/nature04984

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