James R. Garey, Organizer

sponsored by AMS, DEDB, DIZ, DSEB and NSF*.

The symposium was held on Friday, January 5th 2001 at the Society for Integrative and Comparative Biology (SICB) meeting in Chicago. 

Most biologists are familiar with only a few of the approximately 40 extant animal phyla such as annelids, arthropods, molluscs, echinoderms and chordates.  How many are familiar with the more obscure groups such as gnathostomulids, kinorhynchs, priapulids and cycliophorans?  This symposium was designed to play a role in renewing interest in the lesser- known animal groups, encourage their use in research and teaching and promote the relevance of high-level systematic studies.   The symposium was restricted to protostomes simply to narrow the scope so that it could be completed in a single day. The participants of the symposium are shown below.  The proceedings of the symposium are slated for publication in the June 2002 issue of   Integrative and Comparative Biology (formerly American Zoologist).

Left to right top row (standing): Ken Halanych, Claus Nielsen, Jen Grenier, Diane Nelson, Reinhardt Kristensen, Tom Shirley, Birger
Neuhas.  Left to right bottom row (sitting): Clint Turbeville, Andreas Schmidt-Rhaesa, Jim Garey, Bob Wallace, Tom Near. Photo
courtesy of Michael S. Robeson.

DISCUSSION AT THE SYMPOSIUM
    At the end of the symposium there was a lengthy discussion concerning lesser-known taxa. This discussion went along for quite some time until the room had to be vacated to make room for another scheduled event.
 
    There appears to be increased interest in utilizing lesser-known groups, and it was agreed that the symposium did a good job bringing together the systematists who study the taxa, and the researchers, particularly the evolutionary-developmental biologists.  Systematists need to make an effort to publish their findings in more accessible journals, and get involved in collaborative work with other researchers that use their animals.  It would also be helpful if cultures of these animals could be made available.  Many cannot currently be cultured and there should be more effort at developing ways of culturing more of them.   There are a number of ways that investigators can get in touch with people who work with these organisms other than the traditional literature.  SICB is currently developing the Bio-Portal (http://sicb.org/faq.php3 ) to put researchers in touch with each other.  The Sloan Foundation has sponsored the Census of Marine Life ( http://www.coreocean.org/censhome.html ) and the Fauna Europaea (http://www.faunaeur.org ) project are other sites where information about researchers studying lesser-known invertebrates can be found.

    The importance of educating students and the faculty who teach invertebrate zoology cannot be overlooked.  One problem is finding drawings and photographs of the lesser-known taxa for educational use.  Jon Houseman at the University of Ottowa is involved in BIODIDAC, a bank of digital images, video, and animations that can be used and adapted for teaching without charge .   Anyone with images to contribute can contact Jon Houseman through the website ( http://biodidac.bio.uottawa.ca/ ).   Many of the lesser-known groups that used to be dumped into the old “Aschelminthes” can now be related to other groups such as Syndermata, Platyzoa, Cycloneuralia, Panarthropoda and Ecdysozoa.  This makes it much easier for students to learn about them, and many of these new ideas are now presented in introductory biology texts (e.g. Campbell and Reece, 2002) and invertebrate zoology texts such as the fourth edition of Biology of the Invertebrates by Pechenik (2000) and the upcoming seventh edition of Invertebrate Zoology by Ruppert and Barnes.

    There appeared to be a consensus that some terms, particularly “Aschelminthes” needs to be dropped from use since it does not represent a monophyletic group.  It was also suggested that the term Polychaeta may no longer be valid because it appears that Polychaeta may be a synonym for Annelida.   If the lophophorates are indeed polyphyletic, and phoronids are simply “shell-less” brachiopods, then use of the term Lophophorata may also need to be discontinued.   Clearly, many taxon names are currently in flux, and the use of the conventional taxonomic levels of absolute hierarchy such as Phylum, Class, Order and Family is inconsistent and troublesome. 

    With all the changes and new ideas in phylogeny, new molecular tools and with the continued discovery of new taxa (for example, Reinhardt Kristensen introduced a new group of animals, the micrognathozoans, at this symposium that were discovered in a freshwater spring in Greenland), there is appears to be a strong interest in continuing this symposium at approximately five year intervals, perhaps rotating different taxa at different meetings..

HISTORY OF THE SYMPOSIUM AND A TRIBUTE TO ROBERT P. HIGGINS 
    This symposium was organized in response to requests and inquiries from a number of people after the 1998 SICB symposium on Metazoan evolution (McHugh and Halanych, 1998).  The symposium has a history going back to 1976 when Robert Higgins organized a refresher course on the lesser-known invertebrates at a  joint meeting of the  American Institute of Biological Sciences and the American Microscopical Society (AMS) that took place in New Orleans in 1976, and most recently in 1990 at a joint meeting of the American Society of Zoologists and the AMS in San Antonio that was also organized by Higgins.  He has been instrumental in promoting the lesser-known taxa over the years.  As a graduate student, he was present at the well-known symposium on the “Lower Metazoa” in Berkeley (see Dougherty et al.  1963)  that took place in 1961 and included such noted scientists as Adolf Remane, Peter Ax, and others.  Higgins had a long career at the Smithsonian Institute, was very active in the American Society of Zoologists (now SICB) and played a major role in the discovery of the phylum Loricifera.   Despite being  retired, Bob Higgins was invited to speak at this symposium, and although he was unable to attend, he coauthored a contribution with Birger Neuhaus in these proceedings on kinorhynchs.

Time                   Speaker                                          Topic
8:00 - 8:30         Garey                                              Introduction to the lesser-known protostome taxa
8:30 - 9:00         Neuhas                                           Kinorhyncha
9:00 - 9:30         Schmidt-Rhaesa                              The two dimensions of Biodiversity research
                                                                                    exemplified by Nematomorpha and Gastrotricha
9:30 - 10:00        Shirley                                            Priapulida
Coffee
10:20- 11:00       Kristensen                                     An introduction to Loricifera, Cycliophora
                                                                                   and Micrognathozoa
11:00 - 11:30      Nelson                                          Current status of the Tardigrada
11:30 - 12:00      Grenier                                          Minor phyla fill the gaps: Priapulida and Onychophora
Lunch
1:00 - 1:30         Wallace                                           Rotifers: exquisite metazoans
1:30 - 2:00         Near                                               Acanthocephala
2:00 - 2:30         Halanych, McHugh, Dahlgren          Evidence that some lesser-known "phyla are annelids
Coffee
3:20 - 4:00         Nielsen                                            The phylogenetic position of Entoprocta,
4:00 - 4:30         Turbeville                                        Recent progress in Nemertean biology
4:30 - 5:00         Garey                                             Wrap up and Discussion

* This material is based upon work supported by the National Science Foundation under Grant No. 0090638.  Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.

About the Speakers (not alphabetical):

James R. Garey,   University of South Florida- I study the evolutionary relationships of invertebrate animals, mostly with molecular methods (e.g. Winnepenninckx, et al. 1995, Aguinaldo et al. 1997, Garey et al., 1996) but also combined approaches using molecules and morphology (e.g. Schmidt-Rhaesa et al. 1998, Cameron, Garey and Swalla 2000).  I will present an overview of  metazoan phylogeny with emphasis on the lesser known taxa and the controversy between the competing Articulata and Ecdysozoa hypotheses of metazoan evolution.

Robert Higgins, Smithsonian Museum - Bob Higgins is a well known authority on many lesser known groups including Loricifera (Higgins and Kristensen 1986),  priapulids (Storch and Higgins 1991) and kinorhynchs (Higgins 1990) and is retired from the Smithsonian Museum.   He previously organized symposia similar to this one in the 1970's. He will present an historical perspective on the study of lesser known taxa and then focus on the kinorhynchs.

Andreas Schmidt-Rhaesa, University of Bielefeld (Germany) - Andreas Schmidt-Rhaesa is an expert on nematomorphs (e.g. Schmidt-Rhaesa 1997) but also an expert on the morphology and evolution of many of the lesser known groups. He will present a general overview of nematomorphs and also describe how the gastrotrichs are an important taxon because they are considered to be closely related to the molting non-panarthropods and yet they themselves do not molt.

Reinhardt Kristensen, University of Copenhagen (Denmark) - He is the discoverer of several new phyla including Loricifera (Kristensen 1983), Cycliophora (Funch and Kristensen 1995), and now a new group, Micrognathozoa (Kristensen, personal communication).  He will speak on Loricifera, Cycliophora and introduce the new taxon Micrognathozoa which will include a discussion of Gnathostomulida.

Diane Nelson, East Tennessee State University - She is a well-known tardigrade expert in the United States and has studied the ecology (e.g. Nelson and Marley 2000) and systematics (Nelson 1991) of tardigrades throughout her career and will speak on aspects of the ecology and systematics of tardigrades.

Thomas Shirley, University of Alaska   - Tom is well known in the field of meiofauna and has recently described a new priapulid species (Shirley and Storch 1999).  He will speak on the importance of priapulids in the fossil record and the impact of modern priapulids in benthic ecology.

Robert Wallace , Ripon College - He is an expert in the ecology and systematics of benthic tube dwelling rotifers (e.g. Felix, Stevens and Wallace 1995) and has published cladistic analyses of metazoan phylogeny (Wallace, Ricci and Melone 1996). He will speak on the importance of rotifers in freshwater ecology and address the controversy of whether or not acanthocephalans should be included as members of Rotifera.

Thomas Near, University of California, Davis - Tom  is now a postdoctoral fellow at the University of California at Davis and is a very promising young systematist.  He became interested in Acanthocephalans as a Master’s student and has authored several papers on the systematics of acanthocephalans (e.g. Near, et al., 1998).  Tom will speak on the co-evolution of acanthocephalans with their hosts and will address the controversy of whether or not acanthocephalans are members of Rotifera.

Clint Turbeville, University of Arkansas- Clint Turbeville is most well known for his definitive morphological and molecular studies that proved that nemerteans are protostomes not related to flatworms (Turbeville et al. 1992) and was a co-discoverer of Ecdysozoa (Aguinaldo et al. 1997).  He will speak on the ecology and systematics of nemerteans and discuss new insights based on mitochondrial genome sequencing.

Jen Grenier, University of Wisconsin - Jen Grenier is currently a post-doctoral fellow at EraGen Biosciences in Madison WI.  She has worked in the lab of Sean Carroll and carried out ground breaking studies of the evolution of hox genes (e.g. Grenier and Carroll 2000).  She has used onychophorans for much of her work and will address developmental aspects of onychophorans and why they and other lesser known taxa are useful in understanding the evolution of developmental patterning.

Claus Nielsen, University of Copenhagen (Denmark)- Claus Nielsen is best known for his book on animal evolution (Nielsen 1995).  Claus is a master of morphological studies of metazoan evolution.  His specialty has been the entoprocts and lophophorate groups which he will address in this symposium.  He will present arguments that lophophorates are not protostomes, and  should continue to be considered basal deuterostomes.

Ken Halanych, Damhnait McHugh and Thomas Dahlgren, Ken Halanych is currently at Woods Hole Oceanographic Institute and has carried out studies involving several lesser-known groups such as chaetognaths, pterobranchs and hydrothermal vent worms.  He was a co-discoverer of Lophotrochozoa, a group of non-molting protostomes that includes annelids, molluscs and lophophorates (see Halanych et al. 1995, Halanych et al. 1998).  Thomas Dahlgren is a graduate student in Ken Halanych's lab who studies polychaetes (Dahlgren 1996).  Damhnait McHugh is at Colgate University and is an expert on the phylogeny of annelids and their allies (e.g. see McHugh 1997).  They will speak on the relationship of many of these allied taxa, some of which are now thought to be derived polychaetes. This should address the confusion many people have about these taxa because of the many revisions of their phylogenetic relationships.  The presentation will  include Echiurans, pogonophorans, vestimentiferans, and sipunculans and will serve as an introduction to the presentation of Alissa Arp..

Alissa Arp, San Francisco State University - She is well known for her pioneering work on sulfide metabolism of hydrothermal vent worms (Arp and Childress 1983) and more recently in echiuran worms (e.g. Menon and Arp 1998).  Her talk will focus on the interesting physiological and ecological aspects of echiuran worms and why these groups are important to study. 

Aguinaldo A.M.A., Turbeville J.M., Linford L.S., Rivera M.C., Garey J.R., Raff R.A.and Lake J.A. (1997) Evidence for a clade of nematodes, arthropods and other moulting animals.  Nature 387: 489-493.

Arp,  A.J., and J.J. Childress (1983) Sulfide Binding by the Blood of the  Hydrothermal Vent Tube Worm Riftia-pachyptila.  Science 219: 295-297.

Cameron, C.B., Garey, J.R. and Swalla, B.J. (2000). Evolution of the Chordate Body Plan: New Insights from phylogenetic analyses of deuterostome phyla.  Proc. Natl. Acad. Sci. U.S.A. 95:4469-4474.

Dahlgren T. G. 1996. Two new species of Dysponetus (Polychaeta: Chrysopetalidae) from Italy and Papua New Guinea. Proceedings of the Biological Society of Washington 109(3):575-585.

Felix, A., Stevens, M.E. and R.L. Wallace (1995) Unpalatability of a colonial rotifer, Sinantherina socialis to small zooplanktivorous fishes. Invert. Biol. 114:139-144.

Funch, P., and R.M. Kristensen (1995) Cycliophora is a new phylum with affinities to Entoprocta and Ectoprocta, Nature 378:711-714.

Garey J.R., Near T.J., Nonnemacher M.R., and Nadler S.A. 1996.  Molecular evidence for Acanthocephala as a sub-taxon of Rotifera. J. Mol. Evol.  43: 287-292.

Garey, J.R. and Schmidt-Rhaesa, A. (1998).  The essential role of “minor” phyla in molecular studies of animal evolution.  Amer. Zool. 38: 907-917.

Halanych, K.M., J. Bachelor, A.M. Aquinaldo, S. Liva, D.M. Hillis, and J.A. Lake. 1995. 18S rDNA evidence that the lophophorates are
protostome animals. Science 267: 1641-1643.

Halanych, K.M., and R.A. Lutz, and R.C. Vrijenhoek. 1998. Evolutionary origins and age of vestimentiferan tube worms. Cahiers de
Biologie Marine 39: 355-358.

Grenier, J.K. and S.B. Carroll (2000) Functional evolution of the Ultrabithorax protein, Proc. Natl. Acad. Sci. USA 97:704-709.

Higgins, R.P. and R.M. Kristensen (1986) New Loricifera from southeastern United States coastal waters. Smithsonian contributions to Zoology, number 438, 70 pp.

Higgins, R.P. (1990) Zelinkaderidae, a new family of cyclorhagid kinorhyncha. Smithsonian contributions to Zoology, number 500, 26 pp.

Kristensen, R.M. (1983) Loricifera, a new phyhlum with aschelminthes characters from the meiobenthos.  Zeitschrift fur Zoologische Systematik und Evolutionforschung 21:163-180.

McHugh, D. 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. Natl. Acad. Sci. USA 94:8006-8009.

Menon,  J. and A.J. Arp  (1998) Ultrastructural evidence of detoxification in the alimentary canal of Urechis caupo, Invert. Biol. 117: 307-317.

Near, T.J., Garey, J.R., Nadler, S.A. (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molec. Phyl. Evol. 10: 287-298.

Nelson, D.R.  (1991)  Tardigrada, p 501-521.  In: Ecology and Classification of North American Freshwater Invertebrates (J.H. Thorpe, A.P. Covich, eds.).  Academic Press, New York.

Nelson, D.R. and N.J. Marley (2000) The biology and ecology of lotic Tardigrada, Freshwater Biology 44: 93-108.

Nielsen, C. 1995. Animal Evolution. Oxford University Press, Oxford, 467 pp.

Schmidt-Rhaesa, A. (1997) Nematomorpha, Gustav Fischer Verlag, Stuttgart, Germany, 124 pp.

Schmidt-Rhaesa, A., Ehlers, U. Bartolomaeus, T, Lemburg, C. and Garey, J.R. (1998) The phylogenetic position of the Arthropoda.  J. Morphol. 238:263-285.

Shirley, T.C. and V. Storch (1999) Volker Halicryptus higginsi n.sp. (Priapulida): A giant new species from Barrow, Alaska. Invert. Biol. 118: 404-413.

Storch V. and R.P. Higgins (1991) Scanning and transmission electron microscopic observations on the larva of Halicryptus spinuylosus (Priapulida), J. Morph. 210:175-194.

Turbeville JM, Field KG, and Raff  RA (1992) Phylogenetic position of phylum Nemertini, inferred from 18S rRNA sequences: molecular data as a test of morphological character homology. Mol. Biol. Evol. 9:235-249.

Wallace, R.L., C. Ricci and G. Melone. 1996. A cladistic analysis of pseudocoelomate (aschelminth) morphology. Invertebrate Biology 115:104-112.

Winnepenninckx, B., Backeljau, T., Mackey, L.Y., Brooks, J.M., De Wachter, R., Kumar, S. and  Garey, J.R. (1995) 18S rRNA data indicate that the aschelminthes are polyphyletic and consist of at least three distinct clades.  Molec. Biol. Evol. 12: 1132-1137.