PerspectiveDevelopmental Biology

The Ups and Downs of a Sea Anemone

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Science  28 May 2004:
Vol. 304, Issue 5675, pp. 1255-1256
DOI: 10.1126/science.1099829

Sea anemones, corals, and jellyfish [HN1] have had a much-maligned history. Aristotle considered them “zoophytes”: neither animals nor plants, yet having characteristics of both [HN2]. Similar views persisted for more than 2000 years. For example, Charles Bonnet's [HN3] 1799 Scala Naturae or Chain of Being (1) placed sea anemones just above plants and below tapeworms. He thought corals even more primitive, situated far below plants and only marginally above asbestos. Zoologists may shudder at such overtly hierarchical classification schemes, yet the dominant view today is not that different. Most animals—from worms to whales, and flies to foxes—comprise an evolutionary lineage called the Bilateria [HN4]. Sometimes loosely termed “higher animals,” bilaterians have front and rear ends (anterior and posterior), an up-and-down axis (dorsal and ventral), and a plane of mirror symmetry running between the left and right sides (bilateral symmetry). In contrast, sea anemones and their kin (phylum Cnidaria [HN5]) diverged earlier in animal evolution, supposedly before the invention of bilateral symmetry [HN6]. These animals exhibit a simpler form of symmetry termed “radial” symmetry. On page 1335 of this issue, Finnerty and colleagues (2) [HN7] present evidence suggesting it is time to rethink the origins of bilateral symmetry.

Finnerty and co-workers report their study of the starlet sea anemone, Nematostella vectensis [HN8] (see the figure), a member of the basal cnidarian class Anthozoa. This sea anemone has unusual habits that would have confused Aristotle, Bonnet, and the early naturalists. Whereas most sea anemones stick to rocks, looking rather like flowers yet capturing and devouring prey, N. vectensis burrows through the mud of brackish lagoons and estuaries in North America and southern England. A cross section of the adult shows not radial symmetry, as dogma would predict, but a plane of bilateral symmetry (known as the “directive axis”) that traverses the pharynx at right angles to the primary oral-aboral (mouth-foot) body axis. This is not an oddity of Nematostella, but a characteristic of sea anemones. The bilateral symmetry of anthozoans (and not other cnidarians) was noted by Hyman (3) [HN9], an influential invertebrate zoologist of the 20th century, but failed to become a part of common zoological knowledge. If sea anemones possess bilateral symmetry, is it homologous to our own bilateral symmetry or did it arise by convergent evolution? In other words, did bilateral symmetry originate earlier in our ancestry than is commonly believed or did anthozoans evolve from a radial ancestor and develop bilaterality independently?

Stars and stripes.

The starlet sea anemone, Nematostella vectensis, is a cnidarian that is not radially symmetrical but exhibits bilateral symmetry (2). Bilateral symmetry may have evolved before the split between bilaterians and cnidarians. [Adult N. vectensis are ∼2 cm in length.]

CREDIT: JOHN R. FINNERTY/BOSTON UNIVERSITY

Homology [HN10] can be investigated by comparison of gene-expression patterns. If the same genes are used to control development of a structure (or axis) in two morphologically different animals, this lends support to the hypothesis of homology although it does not prove it. The Hox gene cluster [HN11] is the canonical set of genes implicated in control of the anterior-posterior axis in bilaterians. As for the dorsoventral axis, the dpp or bone morphogenetic protein 2/4 gene [HN12] is pivotal for marking the dorsal side in arthropods or the ventral side in vertebrates. In flies, nematodes, vertebrates, and the basal chordate, amphioxus, Hox genes are expressed in staggered (nested) domains from the head to the tail, and instruct appropriate patterns of cell differentiation. Finnerty and co-workers report that in the planula larval stage of Nematostella, five Hox genes are expressed in staggered domains reminiscent of their expression patterns in bilaterians. As for dpp, the Nematostella gene is asymmetrically expressed to one side of the blastopore [as previously described in coral (4)] and later the pharynx. It therefore marks an axis at right angles to the one displaying nested Hox gene expression. These data suggest that the main oral-aboral body axis of a sea anemone, running from mouth to foot, is homologous to the anterior-posterior axis of bilaterians, whereas a precursor of the dorsoventral axis runs through the directive axis.

If bilateral symmetry arose before the evolutionary divergence of cnidarians and bilaterians, then cnidarians no longer hold the clue to the origin of bilaterality. However, examination of other basal animal taxa, notably Placozoa (Trichoplax) and Porifera (sponges) [HN13], may help to resolve this issue. Furthermore, there is more to being a bilaterian than possessing bilateral symmetry. Cnidaria will undoubtedly prove to be a pivotal phylum for examining the origin of these other characteristics, notably the mesoderm, the through-gut, and the central nervous system.

If sea anemones have body axes homologous to ours, which end is which? The Nematostella Hox gene expressed closest to the embryonic blastopore (site of the future mouth) is anthox6, a gene related to anteriorly expressed Hox genes (such as Drosophila labial or mouse Hoxa1, Hoxb1, and Hoxd1) in the Bilateria. Surprisingly, the planula larva swims with this end at the rear. At the opposite end of the animal, where the sea anemone foot will form, is anthox1, a gene related to bilaterian “posterior” Hox genes (such as Drosophila Abd-B). So is the mouth of the sea anemone homologous to the anterior end of a fly or human, and the sea anemone foot homologous to the posterior end? This may be the case, although certain caveats apply. First, the expression patterns of the three other Nematostella Hox genes are hard to interpret, because they are almost coincident rather than staggered. Second, Hox gene-expression patterns differ among cnidarian species. For example, a homolog of an “anteriorly” expressed Hox gene is expressed at the opposite end of the planula larva in the hydrozoan Podocoryne (5) [HN14]. Third, and most important, it is not yet known if the five Nematostella Hox genes are arranged in one genomic cluster, like the Hox genes of the Bilateria. Such information would greatly aid comparison to bilaterian animals. This last point may be resolved soon: The 320-million-base pair genome of N. vectensis is due to be sequenced this year by the U.S. Department of Energy's Joint Genome Institute (6) [HN15].

HyperNotes Related Resources on the World Wide Web

General Hypernotes

Dictionaries and Glossaries

The On-line Medical Dictionary is provided by CancerWeb.

The Life Sciences Dictionary is provided by the BioTech Web site of the University of Texas Institute for Cellular and Molecular Biology.

The Dictionary of Cell and Molecular Biology is made available by the editor, J. Dow, Institute for Biomedical and Life Sciences, University of Glasgow.

A glossary of developmental biology is provided by S. Scadding, Department of Zoology, University of Guelph, Canada.

A glossary is provided by Animal Diversity Web from the University of Michigan Museum of Zoology.

Web Collections, References, and Resource Lists

The Google Directory provides links to Internet resources related to developmental biology.

The Virtual Library-Developmental Biology is maintained by the Society for Developmental Biology (SDB). The Interactive Fly, made available by SDB, is a guide to Drosophila genes and their roles in development, with information about homologous genes in other species.

The WWW Virtual Library of Cell Biology includes sections of Internet links for gene expression and cellular aspects of development.

The Virtual Library on Genetics is sponsored by the Office of Science, Office of Biological and Environmental Research, and Human Genome Program of the U.S. Department of Energy (DOE).

S. Scadding's Developmental Biology Online is a supplemental education resource. Links to Internet resources on developmental biology and cell biology are included.

Online Texts and Lecture Notes

The University of California Museum of Paleontology (UCMP) presents Web exhibits about living and fossil organisms, phylogeny, and evolution.

The Cnidaria Home Page is maintained by R. Steele, Department of Biological Chemistry, University of California, Irvine.

Virtual Embryo/Dynamic Development is a Web resource provided by L. Browder, Department of Biochemistry and Molecular Biology, University of Calgary.

The UNSW Embryology Web site is an educational resource on embryological development provided by M. Hill, School of Anatomy, University of New South Wales, Australia. A section on molecular development is included.

DevBio is the Web supplement for the seventh edition of Developmental Biology by S. Gilbert, Department of Biology, Swarthmore College, PA. A searchable text of the sixth edition of Developmental Biology is available on the NCBI Bookshelf.

R. Fox, Department of Biology, Lander University, Greenwood, SC, provides lecture notes for a course on invertebrate zoology.

J. Houseman, Department of Biology, University of Ottawa, provides lecture notes for a course on animal form and function and lecture notes for a course on invertebrate zoology.

The Department of Biology, University College London, makes available lecture notes for a course on the biology of development.

W. Powell, Biology Department, Kenyon College, OH, offers lecture notes for a course on genetics and development.

General Reports and Articles

R. Merks, Biocomplexity Institute, Indiana University, makes available his Master's degree thesis titled “The molecular Bauplan.”

The 1 April 1992 issue of the Biological Bulletin had an article (full text available in PDF format) by C. Hand and K. Uhlinger titled “The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis.” The 1 August 1997 issue had an article by J. R. Finnerty and M. Q. Martindale titled “Homeoboxes in sea anemones (Cnidaria; Anthozoa): A PCR-based survey of Nematostella vectensis and Metridium senile.”

The 15 May 2004 issue of Development had an article by M. Q. Martindale, K. Pang, and J. R. Finnerty titled “Investigating the origins of triploblasty: ‘Mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa).”

The 22 December 1998 issue of the Proceedings of the National Academy of Sciences had an article by A. G. Collins titled “Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence.” The 25 April 2000 issue (with a special section on evo-devo biology) had an article by K. J. Peterson and E. H. Davidson titled “Regulatory evolution and the origin of the bilaterians.”

Numbered Hypernotes

1. Entries for sea anemones, corals, and jellyfish are included in the Britannica Concise Encyclopedia.

2. Aristotle's classification. L. Donnelly's Anatomy Page offers a profile of Aristotle and his zoological studies. UCMP has a presentation on Aristotle that discusses his classification of animals. D. Likely, Department of Psychology, University of New Brunswick, offers a presentation on Aristotle's taxonomy for a course on the history of psychology. A presentation on Aristotle's classification of animals is provided by the Archaeonia Web site.

3. An entry on Charles Bonnet is included in Wikipedia. The Who Named It? Web site has a profile of Charles Bonnet. D. Likely provides an outline of Bonnet's classification in a presentation on evolution for a course on the history of psychology.

4. Bilateria. A definition of Bilateria is provided by Science's Tree of Life Web feature. Wikipedia provides an introduction to Bilateria. Kimball's Biology Pages offer an introduction to the Bilaterians. The Tree of Life Web project has an entry for Bilateria. A presentation on the Bilateralia is provided by the Palæos Web site. R. Fox provides lecture notes on Bilateria for a course on invertebrate zoology. A. R. Palmer, Department of Biological Sciences, University of Alberta, offers an introduction to the Bilateria for an invertebrate zoology course.

5. Cnidaria. An entry on Cnidaria is included in the Columbia Encyclopedia. UCMP provides an introduction to Cnidaria. The Tree of Life provides information on Cnidaria. Palæos offers a presentation on Cnidaria. J. Houseman makes available lecture notes on Cnidaria for a course on course on animal form and function. R. Fox provides lecture notes on Cnidaria and Cnidaria images for a course on invertebrate zoology. A. R. Palmer provides lecture notes on Cnidaria for an invertebrate zoology course. CnidBase is the Cnidarian Evolutionary Genomics Database; a collection of links are provided.

6. Radial and bilateral biological symmetry. An introduction to biological symmetry is provided by the Columbia Encyclopedia. An introduction to animal body plans is available in the lab notes for a biology course offered by the Department of Biology, San Francisco State University. Wikipedia has entries for bilateral and radial symmetry. R. Irwin, Department of Biological Sciences, University of Tennessee at Martin, offers a presentation on radial versus bilateral symmetry. An introduction to animal symmetry and anatomical terms is provided in a zoology tutorial presented by W. Monaco. A. R. Palmer offers a presentation titled “Breaking symmetry: Eclectic reflections on biological asymmetry.” K. Simmons, Department of Biology, University of Winnipeg, offers lecture notes on the Radiata-Bilateria split for a course on evolution, ecology, and biodiversity.

7. John R. Finnerty and Pat Burton are in the Department of Biology, Boston University. Kevin Pang, Dave Paulson, and Mark Q. Martindale are at the Kewalo Marine Laboratory, Pacific Biomedical Research Center, University of Hawaii.

8. Nematostella vectensis (Class Anthozoa). An introduction to the Anthozoa is provided by UCMP. The Tree of Life provides information about Anthozoa and sea anemones (with an illustration of Nematostella. vectensis). MarLIN (Marine Life Information Network for Britain and Ireland) provides information about the Starlet sea anemone Nematostella vectensis. The National Biodiversity Network's Species Dictionary, from the Natural History Museum, London, provides information about N. vectensis. The Encyclopedia of Marine Life of Britain and Ireland, provided by the HabitasOnline Web site of the Ulster Museum Sciences Division, has an entry for N. vectensis.

9. A brief profile of Libbie Hyman is offered by the Encyclopedia Britannica's Woman in American History Web site. Wikipedia has a biographical entry about Libbie Hyman. The National Academy of Sciences' Biographical Memoirs (Vol. 60,1991) includes an autobiographical essay by Hyman and an essay on her scientific work by G. E. Hutchinson.

10. Homology is defined by the Columbia Encyclopedia. C. Kimmel, Department of Biology, University of Oregon, offers lecture notes on homology for a course on vertebrate evolution and development. S. Gilbert's Zygote Web site includes a presentation on homologies of process. A. Martin, Department of Ecology and Evolutionary Biology, University of Colorado, offers lecture notes on homology, orthology, homoplasy, and paralogy for a course on molecular evolution and systematics.

11. The Hox gene cluster and the anterior-posterior axis in bilaterians. An introduction to Hox genes is included in a student project on Drosophila prepared for a Princeton University course on biotechnology and its social impact. M. Hill's UNSW Embryology has a presentation on the Hox family and development. C. Kimmel offers lecture notes on Hox genes and anterior-posterior patterning for a course on vertebrate evolution and development. L. Browder's Dynamic Development offers lecture notes by D. Rancourt on Hox genes in vertebrate development. E. De Robertis, Howard Hughes Medical Institute, University of California, Los Angeles, provides (in PDF format) lecture notes on Hox genes and the evolution of animal design. D. Godt, Department of Zoology, University of Toronto, provides lecture notes on Hox genes and pattern formation in insects and vertebrates for a course on developmental biology. Nature Reviews Genetics makes available a slide presentation of the illustrations from the January 2001 article by D. E. K. Ferrier and P. W. H. Holland titled “Ancient origins of the Hox gene cluster.” The HOX DataBase is provided by A. Spirov, Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg.

12. The genes dpp and bone morphogenetic protein 2/4. Entries for dpp and bone morphogenetic protein (BMP) are included in H. Ibelgaufts' Cytokines Online Pathfinder Encyclopaedia (COPE). GeneCards has entries for BMP2 and BMP4 genes with links to other resources. R&D Systems provides a review of BMPs. The Interactive Fly has a review of dpp in Drosophila with a section on evolutionary homologs. A. Spirov's Gene Networks Database provides information on dpp in Drosophila development. FlyMove offers a presentation on dpp and dorsal-ventral development in Drosophila. The 11 June 2002 issue of the Proceedings of the National Academy of Sciences had an article by D. C. Hayward et al. titled “Localized expression of a dpp/BMP2/4 ortholog in a coral embryo” (4). D. Godt provides lecture notes on dorsal-ventral pattern formation in flies and frogs for a course on developmental biology.

13. Placozoa (Trichoplax) and Porifera. UCMP provides introductions to Placozoa and Porifera. Animal Diversity Web provides an introduction to Porifera. An introduction to the Placozoa is provided by a Columbia University course on the life system. An article about Trichoplax by R. L. Howey is available on the Microscopy-UK Web site. For a seminar on the collections of the Peabody Museum, L. Buss, Department of Ecology and Evolutionary Biology, Yale University, makes available in PDF format an article by T. Syed and B. Schierwater titled “Trichoplax adhaerens: Discovered as a missing link, forgotten as a hydrozoan, re-discovered as a key to metazoan evolution.” The January 2000 issue of Molecular Biology and Evolution had an article by Andrea Ender and B. Schierwater titled “Placozoa are not derived Cnidarians: Evidence from molecular morphology.”

14. Hydrozoan Podocoryne. An introduction to the Hydrozoa is provided by UCMP. V. Schmid, Institute of Zoology, University of Basel, provides an illustrated presentation about Podocoryne carnea and his research. The Hydrozoan Society provides links to Internet resources on Hydrozoa.

15. The DOE Joint Genome Institute is operated by the University of California for the U.S. Department of Energy. The International Sequencing Consortium lists large-scale sequencing projects sorted by organisms. An 8 April 2004 posting by R. Steele to the Cnidaria Newsgroup provides an update on Nematostella genomics efforts.

16. Peter Holland is in the Department of Zoology, University of Oxford.

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