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Cephalopod Hox genes and the origin of morphological novelties

Nature volume 424, pages 1061–1065 (2003)Cite this article

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.

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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.

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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L. Nederbragt, D. Matus, K. Pang and L. Kaneshige for critical reading of the manuscript; B. Degnan for sharing unpublished data; S. v. Boletzky for sending us reprints of many cephalopod developmental studies; and M. McFall-Ngai for providing additional embryos.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.

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Authors and Affiliations

  1. Department of Zoology, University of Hawaii at Manoa, 2538 McCarthy Mall, Honolulu, Hawaii, 96822, USA

    Patricia N. Lee & Heinz G. de Couet

  2. Kewalo Marine Laboratory/Pacific Biomedical Research Center, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii, 96813, USA

    Patricia N. Lee & Mark Q. Martindale

  3. Department of Biology & Biochemistry, University of Houston, 369 Science and Research Bldg 2, Houston, Texas, 77204, USA

    Patrick Callaerts

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Correspondence to Heinz G. de Couet.

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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

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