Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Cephalopod Hox genes and the origin of morphological novelties

Abstract

Cephalopods are a diverse group of highly derived molluscs, including nautiluses, squids, octopuses and cuttlefish. Evolution of the cephalopod body plan from a monoplacophoran-like ancestor1 entailed the origin of several key morphological innovations contributing to their impressive evolutionary success2. Recruitment of regulatory genes3, or even pre-existing regulatory networks4, may be a common genetic mechanism for generating new structures. Hox genes encode a family of transcriptional regulatory proteins with a highly conserved role in axial patterning in bilaterians5; however, examples highlighting the importance of Hox gene recruitment for new developmental functions are also known6,7. Here we examined developmental expression patterns for eight out of nine Hox genes8 in the Hawaiian bobtail squid Euprymna scolopes, by whole-mount in situ hybridization. Our data show that Hox orthologues have been recruited multiple times and in many ways in the origin of new cephalopod structures. The manner in which these genes have been co-opted during cephalopod evolution provides insight to the nature of the molecular mechanisms driving morphological change in the Lophotrochozoa, a clade exhibiting the greatest diversity of body plans in the Metazoa.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Cephalopod evolution and body plan.
Figure 2: Evolution of the cephalopod brain and Hox expression in the CNS.
Figure 3: Hox expression in the developing brachial crown.
Figure 4: Hox expression in the stellate ganglia.
Figure 5: Individual Hox expression in metabrachial vesicles, buccal crown and light organ.

References

  1. Runnegar, B. & Pojeta, J. J. Molluscan phylogeny: the paleontological viewpoint. Science 186, 311–317 (1974)

    ADS  CAS  Article  Google Scholar 

  2. House, M. R. in Cephalopods—Present and Past (eds Wiedmann, J. & Kullmann, J.) 1–16 (Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, 1988)

    Google Scholar 

  3. Lowe, C. J. & Wray, G. A. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389, 718–722 (1997)

    ADS  CAS  Article  Google Scholar 

  4. Keys, D. N. et al. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283, 532–534 (1999)

    ADS  CAS  Article  Google Scholar 

  5. Carroll, S. B., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design (Blackwell Science, Malden, 2001)

    Google Scholar 

  6. Telford, M. J. Evidence for the derivation of the Drosophila fushi tarazu gene from a Hox gene orthologous to lophotrochozoan. Lox5. Curr. Biol. 10, 349–352 (2000)

    CAS  Article  Google Scholar 

  7. Godwin, A. R. & Capecchi, M. R. Hoxc13 mutant mice lack external hair. Genes Dev. 12, 11–20 (1998)

    CAS  Article  Google Scholar 

  8. Callaerts, P. et al. HOX genes in the sepiolid squid Euprymna scolopes: implications for the evolution of complex body plans. Proc. Natl Acad. Sci. USA 99, 2088–2093 (2002)

    ADS  CAS  Article  Google Scholar 

  9. Brusca, R. C. & Brusca, G. J. Invertebrates (Massachusetts, Sinauer, Sunderland, 2003)

    Google Scholar 

  10. Boletzky, S. v. in Cephalopods—Present and Past (ed. Wiedmann, J. K., J.)) 167–179 (Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, 1988)

    Google Scholar 

  11. Budelmann, B. U. in The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach (eds Breidbach, O. & Kutsch, W.) 115–138 (Birkhauser, Basel, 1995)

    Book  Google Scholar 

  12. Hinman, V. F., O'Brien, E. K., Richards, G. & Degnan, B. M. Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evol. Dev. (in the press)

  13. Shigeno, S., Kidokoro, H., Tsuchiya, K., Segawa, S. & Yamamoto, M. Development of the brain in the oegopsid squid, Todarodes pacificus: an atlas up to the hatching stage. Zool. Sci. 18, 527–541 (2001)

    Article  Google Scholar 

  14. Shigeno, S., Tsuchiya, K. & Segawa, S. Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. J. Comp. Neurol. 437, 449–475 (2001)

    CAS  Article  Google Scholar 

  15. Hartmann, B. et al. Pax6 in the sepiolid squid, Euprymna scolopes: evidence for a role in eye, sensory organ and brain development. Mech. Dev. 120, 177–183 (2003)

    CAS  Article  Google Scholar 

  16. Boletzky, S. v. McGraw-Hill Yearbook of Science & Technology 73–76 (McGraw-Hill, New York, 1994)

    Google Scholar 

  17. Young, J. Z. The organization of a cephalopod ganglion. Phil. Trans. R. Soc. Lond. B 263, 409–429 (1972)

    ADS  CAS  Article  Google Scholar 

  18. Boletzky, S. v., Frösch, D. & Mangold, K. Développement de vésicules associées au complexe brachial chez les Céphalopodes. C.R. Acad. Sci. (Paris) D 270, 2182–2184 (1970)

    Google Scholar 

  19. Sundermann, G. Development and hatching state of ectodermal vesicle-organs in the head of Sepia officinalis, Loligo vulgaris, and Loligo forbesi (Cephalopoda, Decabrachia). Zoomorphology 109, 343–352 (1990)

    Article  Google Scholar 

  20. McFall-Ngai, M. & Montgomery, M. The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes Berry (Cephalopoda: Sepiolidae). Biol. Bull. 179, 332–339 (1990)

    CAS  Article  Google Scholar 

  21. Nogi, T. & Watanabe, K. Position-specific and non-colinear expression of the planarian posterior (Abdominal-B-like) gene. Dev. Growth Diff. 43, 177–184 (2001)

    CAS  Article  Google Scholar 

  22. Kulakova, M. A., Kostyuchenko, R. P., Andreeva, T. F. & Dondua, A. K. The Abdominal-B-like gene expression during larval development of Nereis virens (polychaeta). Mech. Dev. 115, 177–179 (2002)

    CAS  Article  Google Scholar 

  23. Zákány, J. & Duboule, D. Hox genes in digit development and evolution. Cell Tissue Res. 296, 19–25 (1998)

    Google Scholar 

  24. Averof, M. & Patel, N. H. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682–686 (1997)

    ADS  CAS  Article  Google Scholar 

  25. Burke, A. C., Nelson, C. E., Morgan, B. A. & Tabin, C. Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995)

    CAS  PubMed  Google Scholar 

  26. Moshel, S. M., Levine, M. & Collier, J. R. Shell differentiation and engrailed expression in the Ilyanassa embryo. Dev. Genes Evol. 208, 135–141 (1998)

    CAS  Article  Google Scholar 

  27. Nederbragt, A. J., van Loon, A. E. & Dictus, W. J. A. G. Expression of Patella vulgata orthologs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. Dev. Biol. 246, 341–355 (2002)

    CAS  Article  Google Scholar 

  28. Wanninger, A. & Haszprunar, G. The expression of an engrailed protein during embryonic shell formation in the tusk-shell, Antalis entalis (Mollusca, Scaphopoda). Evol. Dev. 3, 312–321 (2001)

    CAS  Article  Google Scholar 

  29. Seaver, E. C., Paulson, D., Irvine, S. Q. & Martindale, M. Q. The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev. Biol. 236, 195–209 (2001)

    CAS  Article  Google Scholar 

  30. Holland, C. H. The nautiloid cephalopods: a strange success. J. Geol. Soc. Lond. 144, 1–15 (1987)

    Article  Google Scholar 

Download references

Acknowledgements

We thank D. Paulson for assistance with in situ hybridization protocols; E. Seaver, A. Wikramanayake, L. Nederbragt, D. Matus, K. Pang and L. Kaneshige for critical reading of the manuscript; B. Degnan for sharing unpublished data; S. v. Boletzky for sending us reprints of many cephalopod developmental studies; and M. McFall-Ngai for providing additional embryos. This study was supported by grants from the National Science Foundation to M.Q.M., H.G.d.C. and P.C. Kewalo Marine Laboratory/Pacific Biomedical Research Center, University of Hawaii is the present address of P.N.L.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heinz G. de Couet.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lee, P., Callaerts, P., de Couet, H. et al. Cephalopod Hox genes and the origin of morphological novelties. Nature 424, 1061–1065 (2003). https://doi.org/10.1038/nature01872

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01872

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing