Evolutionary Relationships of Metazoan Phyla ...

AMER. ZOOL., 38:813-817 (1998)

Introduction to the Symposium: Evolutionary Relationships of Metazoan Phyla: Advances, Problems, and Approaches1 DAMHNAIT MCHUGH 2 - 3 - 4 * AND KENNETH M. HALANYCH 4 - 5 !

*Harvard University, Dept. of Organismic and Evolutionary Biology and Museum of Comparative Zoology, 26 Oxford Street, Cambridge, Massachusetts 02138 t Center for Theoretical and Applied Genetics, Rutgers University, 71 Dudley Road, New Brunswick, New Jersey 08901-8521

ed 19 researchers from North America and Europe, acts as a catalyst for coordinated efforts that will promote continued progress in the field.

Where are we? Most of our understanding of metazoan relationships has been based largely on the detailed comparative work of morphologists, such as Libbie Hyman (1940-1967). However, our understanding of metazoan evolution is being changed by recent molecular data, as well as cladistic analyses of morphological data. For example, recent work by Lake and colleagues based on 18S rDNA suggests that molting animals, including nematodes and arthropods, form a monophyletic group, the Ecdysozoa (Aguinaldo et al., 1997). One of the major implications of this hypothesis is that similarities found in the nematode Caenorhabditis elegans and the fruitfly Drosophila melanogaster may be derived features for a clade of metazoans and not ancestral characteristics of bilateral animals. As another example, Balavoine (1997) discussed the organizational similarities of flatworm Hox genes to those of derived protostomes. This work affects how we view the evolution of the metazoan coelom, among other body plan features. Hypotheses such as these are profoundly altering some of our more tra1 From the symposium Evolutionary Relationships of Metazoan Phyla: Advances, Problems, and Ap- ditional views of metazoan relationships, proaches presented at the Annual Meeting of the So- and they serve to stimulate research in other ciety for Integrative and Comparative Biology, 3—7 areas {e.g., comparative studies of molting, January 1998, at Boston, Massachusetts. or ultrastructural studies of coelomic linings). 2 Order of authorship determined by coin toss. 3

E-mail: [email protected] Present address: Department of Biology, Colgate University, Hamilton, NY 13346. 5 Present address: Biology Department, Woods Hole Oceanographic Institute, Woods Hole, MA 02543. 4

During the symposium, reviews of recent molecular work included J. Garey's discussion of several "aschelminth" phyla and B. Winnepenninckx's analysis of 18S rDNA

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For the 1,033,614 species of living animals estimated by Wilson (1988), there are roughly 1 X 106000000 possible unrooted phylogenetic trees. Despite this intimidating possibility, its many biologists have accepted the challenge to try to reconstruct the metazoan tree. The aim of this symposium was to assess the current state of knowledge concerning the evolutionary relationships of animal phyla, to examine potential pitfalls associated with reconstructing metazoan evolution, and to address unresolved issues in metazoan phylogeny. In the ten years since the seminal paper of Field et al. (1988), the number of studies (and corresponding research effort) addressing metazoan phylogeny has increased steadily. This growth reflects the accumulation of morphological and molecular data, as well as the integration of paleontological and developmental data into phylogenetic studies of the Metazoa. With this growing body of data, we (the co-organizers with support from others) felt the need to facilitate interactions, discussions, and debates among paleontologists, molecular systematists, developmental biologists, and comparative morphologists to promote a more coordinated search for "The Phylogeny," Our hope is that this symposium, which includ-

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pod lineages, and C. Wray combined several sources of data, including developmental genetics, to suggest that molluscs show vestiges of segmentation. P. Holland demonstrated that the presence or absence of some Hox gene clusters may be diagnostic of several major metazoan lineages and thus can be useful in determining how these major metazoan lineages are related. These talks complemented another SICB symposium, organized by L. Olsson and B. Hall, which highlighted the importance of evolutionary development research in understanding major transitions in animal body plans. While genetic tools can provide a novel perspective on metazoan history, caution is needed in interpreting the results, esWhat tools work best? pecially when analyzing patterns of gene Field et al. (1988) helped trigger a re- expression across widely divergent taxa. While tools for studying molecular and surgence in higher-level metazoan systematics, and also established 18S rDNA as the morphological diversity of extant organprimary gene used in phylogenetic analyses isms are useful for inferring evolutionary of higher-level metazoan relationships. As history, paleontological data offers the only D. Eernisse, K. Halanych, and several other real glimpses of what actually happened. R. participants mentioned, the use of 18S Mooi's presentation illustrated how fossil rDNA data for phylogeny reconstruction evidence provides the means of discrimihas both positive and negative aspects. Al- nating between competing hypotheses of though data collection of the 18S rDNA has echinoderm origins. In contrast, B. Wagseveral advantageous characteristics {e.g., goner's talk on Ediacaran fauna reminded ease of isolation, concerted evolution, uni- us that despite having glimpses of the past, versal primer sites), analysis of the gene can we still need a context in which remnants be troublesome due to alignment problems of ancient life can be interpreted. However, and unequal rate effects. A consensus has most paleontologists would agree that more emerged that the utility of 18S data is lim- fossil evidence usually allows for easier inited, and that other lines of evidence, es- terpretation. The increasing rate of discovpecially other molecular markers, need to ery and description of fossils from early be explored (McHugh, 1998; Maley and Cambrian and Precambrian deposits {e.g., Marshall, 1998; Abouheif et al., 1998). Bengston and Zhao, 1997; Li et al., 1998; One of the most rapidly growing areas of Xiao et al., 1998) is altering our view on metazoan research is the molecular evolu- the timing of metazoan radiations, and tion of development. Comparative studies gives hope that additional insights will be of gene regulation and expression patterns forthcoming. of transcriptional genes during development can provide important clues to how evolu- Where do we need to go? tionary events on a relatively short time Even though 18S rDNA has been a powscale can influence macroevolutionary pat- erful tool that has reshaped some of our terns. R. Raff showed that larval body plan thoughts on metazoan evolution, additional morphology, as controlled by expression of sources of data must be explored and detranscription factors, can change radically veloped; this is particularly true for molecin very short spans of evolutionary time. L. ular data. Along these lines, J. Regier and Nagy discussed how the study of gene net- D. McHugh both presented work focusing works, not single genes, can provide new on the nuclear protein-coding gene eloninsights into the evolution of major arthro- gation factor-1 a (EF-1 a). Initial work sug-


data, which revealed that the novel Cycliophora may be related to rotifers. Complementary work assessing our current understanding based on morphological evidence was presented by K. Fauchald and C. Nielsen, both of whom highlighted the need to collect information from non-molecular sources. For many taxa, our understanding of morphology, physiology, or embryology is based on one or two well studied species. Both Fauchald and Nielsen illustrated that this limitation can influence our interpretation of evolutionary change. Clearly, just as in molecular studies, our interpretation in any field of biology is largely dependent on the taxa studied.

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sium was to identify those taxa that are particularly problematic for higher-level metazoan phylogeny. Three organismal groups (flatworms, annelids, and "aschelminthes") seem particularly troublesome. In the case of flatworms and annelids, traditional classification schemes may not reflect the phylogenetic diversity within these two groups; as more information has become available, the monophyly of these groups (as traditionally defined) has come into question (e.g., Carranza et al., 1997; McHugh, 1997; Rouse and Fauchald, 1997). As for the "aschelminthes," many workers have shied away from these groups because the body size, availability, and difficult identification of these groups makes them hard to work with. At least for the near future, the best way to deal with these three problematic groups will be to greatly increase taxon sampling. Through this approach, we may be able to more accurately assess issues of monophyly and phylogenetic placement. Future outlook? Initially, reconstructing metazoan phylogeny appears incredibly daunting. However, the prospect of recovering "The Phylogeny" is much more promising than the total number of possible unrooted trees (1 X io6000000) would indicate. For example, it is safe to assume that a sample of many fewer than 1,033,614 species will provide nearly all the available phylogenetic signal for deep branches in the metazoan tree; just how taxonomically inclusive the reconstructions will need to be is not clear. The current problems of reconstructing phylogeny with a large number of taxonomic units are mostly due to limitations of systematic theory and computer resources. Fortunately, advances in both these areas, as well as in molecular data collection, are being made at an impressive pace. Concomitantly, the outlook for reconstructing metazoan evolutionary history is becoming increasingly optimistic. While this surge in technology and theory is very promising, we should not forget the need to thoroughly develop and explore non-molecular data, i.e., neontological and paleontological information. These types of data are of utmost importance, not only as


gests that some findings based on 18S rDNA are supported by analyses of this second gene, whereas others are not. More importantly, EF-la is the first gene, other than the 18S rDNA, for which a concerted effort is underway to encompass animal diversity in phylogenetic analyses (e.g., McHugh, 1997; Regier and Shultz, 1997). The nature and timing of animal diversification was intensively discussed at the symposium. J. Levinton expanded upon the recent paper of Wray et al. (1996), which argued (based on a molecular clock) that the "Cambrian explosion" was a more ancient event, and was more of a long, protracted fizzle than a big bang. S. ConwayMorris defended the explosion theory based on fossil evidence, but conceded that it may have occurred slightly earlier than traditionally believed. K. Halanych asserted that 18S data are consistent with a rapid radiation among protostome taxa (not deuterostomes as used in Wray et al.), but information from additional markers is needed. Following the symposium, an analysis by Ayala et al. (1998) was published arguing that, contra Wray et al. (1996), the molecular clock approach yields estimates very much in line with fossil data (Bengtson, 1998). Disagreement persists on this issue, and the mode and tempo of the "Cambrian explosion" remains a volatile issue that deserves future attention. The structure, arrangement, and organization of genomes is a relatively unexplored source of potential phylogenetic information. J. Boore presented findings that he and his collaborators obtained by comparing mitochondrial gene order across diverse taxa. In particular, mitochondrial gene order appears to provide information on the affinities of several protostome worm taxa. Other groups, such as bivalve molluscs, have undergone such numerous rearrangement events that phylogenetic interpretations are made much more difficult. To date, obtaining such information has required substantial laboratory effort and cost. However, with the increased speed and accuracy of DNA sequencing, genomic-level information will be an important source of phylogenetic signal in the coming years. Another underlying goal of the sympo-

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ACKNOWLEDGMENTS

From the time the idea for this symposium was first conceived, many people have provided much appreciated support, particularly Billie Swalla, Doug Eernisse, and Pat Reynolds. We also thank Jim Hanken and Doug Erwin for their editorial guidance and input. The SICB staff was very helpful in sorting out many logistical matters, and Willy Bemis aided in planning. Funding for the symposium was provided by NSF (DEB 9707146), the SICB general fund, SICB's Division of Systematics and Evolutionary Biology and Division of Invertebrate Zoology.

REFERENCES Abouheif, E., R. Zardoya, and A. Meyer. Limitations of metazoan 18S rRNA sequence data: Implications for reconstructing a phylogeny of the animal kingdom and inferring the reality of the Cambrian explosion. J. Mol. Evol. (In press). Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489-493. Ayala, F. J., A. Rzhetsky, and F. J. Ayala. 1998. Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates. Proc. Nat. Acad. Sci., U.S.A. 95:606-611. Balavoine, G. 1997. The early emergence of platyhelminths is contradicted by the agreement between 18S rRNA and Hox genes data. C. R. Acad. Sci. Paris 320:83-94. Bengtson, S. 1998. Animal embryos in deep time. Nature 391:529. Bengston, S. and Y. Zhao. 1997. Fossilized metazoan embryos from the earliest Cambrian. Science 277: 1645-1648. Bode, H. R. and R. E. Steele. 1989. Phylogeny and molecular data. Science 243:549. Carranza, S., J. Baguiia, and M. Riutort. 1997. Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences. Mol. Biol. Evol. 14(5):485-497. Field, K. G., G. J. Olsen, D. J. Lane, S. J. Giovannoni, M. T. Ghiselin, E. C. Raff, N. R. Pace, and R. A. Raff. 1988. Molecular phylogeny of the animal kingdom. Science 239:748-753. Hyman, L. H. 1940-1967. The invertebrates. McGraw Hill Book Company, Inc., New York. Lecointre, G., H. Philippe, H. L. V. Le, and H. L. Guyader. 1993. Species sampling has a major impact on phylogenetic inference. Mol. Phylo. Evol. 2: 205-224. Li, C.-W., J.-Y. Chen, and T.-E. Hua. 1998. Precambrian sponges with cellular structures. Science 279:879-882. Maley, L. E. and C. R. Marshall. 1998. The coming of age of molecular systematics. Science 279:505— 506. McHugh, D. 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. Nat. Acad. Sci., U.S.A. 94:8006-8009. McHugh, D. 1998. Deciphering metazoan phylogeny: The need for new molecular data. Amer. Zool. 38: 859-866. Nielsen, C. 1989. Phylogeny and molecular data. Science 243:548. Rouse, G. and K. Fauchald. 1997. Cladistics and polychaetes. Zoologica Scripta 26:139-204. Regier, J. C. and J. W. Shultz. 1997. Molecular phylogeny of the major arthropod groups indicates polyphyly of crustaceans and a new hypothesis for the origin of hexapods. Mol. Biol. Evol. 14:902913. Walker, W. F. 1989. Phylogeny and molecular data. Science 243:549. Wilson, E. O. 1988. The current state of biological


additional sources of characters for phylogenetic analyses and in understanding the timing of metazoan diversification, but they are also critical in assessing whether a particular analysis of molecular data or a particular result makes "biological sense." For example, some of the conclusions reached in the initial paper by Field et al. were refuted based on non-molecular information (Nielsen, 1989; Walker, 1989; Bode and Steele, 1989). Given the importance of this type of information, we make an urgent appeal to fellow researchers and funding agencies to make a strong commitment to the training of biologists with a well-rounded understanding of organisms as well as molecules. We would also like to urge the community as a whole to make efforts to maintain communication among laboratories. Because adequate taxon sampling is crucial for accurate phylogeny reconstruction (e.g., Lecointre et al., 1993), communication, collaboration, and interaction is of paramount importance if we are to build topologies representative of all Metazoa for several different genes. Overall, we are confident that the next ten years of higher-level metazoan phylogenetics will clarify immensely our understanding of metazoan history. The research effort has increased, the tools have improved, and we have a clear view of where we are, as well as where we need to go. As our understanding of metazoan evolution increases, the number of possible alternative evolutionary topologies appears to be shrinking.

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diversity. In E. O. Wilson (ed.), Biodiversity, pp. 3-18. National Academy Press, Washington, D. C. Wray, G. A., J. S. Levinton, and L. H. Shapiro. 1996. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274:568573.

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Xiao, S., Y. Zhang, and A. H. Knoll. 1998. Threedimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391:553-558. Corresponding Editor: Douglas H. Erwin
