© 2003 by The Society for Integrative and Comparative Biology
| ||||||||||||||||||||||||||||||||||||||||||||||||||
New Perspectives on the Origin of Metazoan Complexity: An Introduction to the Symposium1
1 Department of Biology, Appalachian State University, Boone, North Carolina 28608
 |
INTRODUCTION |
|---|
TOP
 INTRODUCTION TRIBUTE TO REINHARD M....References |
|---|
Impressive gains have been made in our understanding of metazoan complexity at the molecular level, especially those in the field of developmental evolution, but our understanding at other levels has lagged behind. This symposium attempts to bring diverse perspectives to bear on the causes and mechanisms of the explosive growth in metazoan complexity in the late Precambrian and Lower Cambrian. A primary goal is to broaden the framework for study of animal origins by introducing topics that are often overlooked by comparative biologists. An additional goal is to bring together workers that hold very different views on the early evolution of metazoans. For example, paleontologists and neontologists vary widely in their interpretations of a remarkable assemblage of fossils, the so-called Ediacara biota that existed in the latest Neoproterozoic (600–543 Ma). This assemblage is widely regarded as belonging to a metazoan or premetazoan radiation by paleontologists and yet the construction of these organisms is rarely taken into consideration by neontologists. Very often metazoan ancestors are assumed to have been a simple larva or flatworm-like organism, such as the microscopic acoelomate considered to have been the bilaterian ancestor (see Rieger et al., 1991
) in spite of the fact that many Ediacarans are large frond- or slug-like organisms, and highly modular.
The theory that early metazoans were simple and that complexity has been assembled incrementally is flawed for other reasons. Such a trajectory is not required by logic, because the first metazoans could have been complex, with complexity decreasing in some or most clades. In addition, a "complexity late" scenario provides no clues about the structure of the intermediate forms connecting the simple common ancestor with later more complex forms; indeed, little work of even a speculative nature has been done to address this issue (Conway Morris, 2000). The assumption is also challenged by the discovery that protostomes and deuterostomes share complex developmental programs, such as the Hox cluster regulating spatial patterning (Balavoine and Adoutte, 1998; de Rosa et al., 1999; Holland, 1998), and that even cnidarians possess a complex set of Hox genes (Finnerty and Martindale, 1999; Gauchat et al., 2000; Kourakis and Martindale, 2000). Although genetic complexity usually is thought to have preceded increases in body plan complexity, the possibility that morphological complexity grew concomitantly with or even before (Budd, 1999) diversification of the genome cannot be dismissed. The Cambrian fossil record suggests that many metazoans were macroscopic and adapted for life in the macrobenthos (Gehling, 1991; Dzik, 1993; Fedonkin and Waggoner, 1997; Valentine et al., 1999; Martin et al., 2000). Metazoan characters are more typical of large organisms, and large organisms are likely to be more complex (Bonner, 1988), and the functions, at least of bilaterian characters, indicate that they arose in large organisms (Budd and Jensen, 2000; Dewel, 2000).
The relationship of the Ediacarans to other organisms has been a contentious issue. Hypotheses on what they are range from the interpretation that they fit into metazoan classes and phyla to the assertion that they are not metazoans but are protists or even lichens. Such discrepancy in their interpretation underscores the need to understand, for example, the factors affecting their preservation (Gehling et al., 2000), before testable hypotheses can be formulated. Many questions are begging for an answer. What grades of cellular or tissue organization do they exhibit? Can we demonstrate higher metazoan taxa in the assemblage? What is the relationship between the trace and body fossil record? Are many Ediacarans truly modular? Do they exhibit serial and fractal patterns of growth and the same trends toward higher levels of integration found in colonial organisms? Difficulties in answering these questions have discouraged many biologists from incorporating data from the assemblage into their work. Conversely, while paleontologists have produced significant advances in our understanding of these organisms, this knowledge has not been fully evaluated in the context of recent progress in developmental and molecular biology. If basal metazoans were modular, then their history may have included integration of those modules into a new entity with a higher level of nested hierarchical complexity. Such an event should have left a record in the geno- or phenotypes of living metazoans. The goal of this symposium, therefore, is to expose biologists and paleontologists to both fields of study and by doing so identify promising areas for future research on the origin of metazoan complexity.
|
TRIBUTE TO REINHARD M. RIEGER |
|---|
|
TOP
INTRODUCTIONTRIBUTE TO REINHARD M....References |
|---|
Reinhard M. Rieger has served as an inspiration for the theme of this symposium. As a neontologist he was one of first to recognize the significance of the fossil record and has taken a leadership role in challenging the idea that early metazoan history was hidden in a microscopic realm populated with tiny ancestors. As he wrote in the important book by Simonetta and Conway Morris (1991, p. 109)
, "The question whether the bilaterian stem-species was microscopic, moving by ciliary locomotion and exhibiting direct development or whether it was equipped with a biphasic life cycle with microscopic larva and clonal, macroscopic adult (cm-size range) is particularly relevant in the light of recent advances. These are our knowledge of the Precambrian metazoan fossils such the Ediacaran fauna (see e.g., Glaessner, 1984; Seilacher, 1984; Conway Morris, 1989), new concepts in life history strategies and life cycle evolution (e.g., Stearns, 1982, 1987; Sibly and Calow, 1986), recent arguments about possible evolutionary strategies of asexual versus sexual reproduction and clonal versus aclonal organization (e.g., Boardman et al., 1973; Jackson et al., 1985; Buss, 1987) and, finally, recent advances in evolutionary biomechanics (Alexander, 1988; Wainwright, 1988)."
|
ACKNOWLEDGMENTS |
|---|
Symposium co-organizer Julian Smith and I thank the Society for Integrative and Comparative Biology, American Microscopical Society, and the Paleontological Society for supporting the symposium. We would also like to thank Jim Gehling for his advice in organizing the paleontological portion of the program and John Pearse, Program Officer for SICB, for all his help with planning. Finally, we acknowledge the enthusiastic support given by Larry McEdward before his tragic death. This symposium was supported by the National Science Foundation under Grant No. 0130902 (to Ruth Ann Dewel, Mark Martindale, and Dan McShea).
|
FOOTNOTES |
|---|
1 From the Symposium New Perspectives on the Origin of Metazoan Complexity presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: dewelra{at}appstate.edu
|
References |
|---|
|
TOP
INTRODUCTIONTRIBUTE TO REINHARD M....References |
|---|
Alexander, R. McN. 1988. Elastic mechanisms in animal movement. Cambridge University Press, Cambridge.
Balavoine, G., and A. Adoutte. 1998. One or three Cambrian radiations? Science, 280:397-398.
Boardman, R. S., A. H. Cheetham, and W. A. Oliver.(eds.) 1973. Animal colonies: Development and function through time. Dowden, Hutchinson, and Ross, Stroudsburg.
Bonner, J. T. 1988. The evolution of complexity by means of natural selection. Princeton University Press, Princeton.
Budd, G. E. 1999. Does evolution in body-patterning genes drive morphological change or vice versa? BioEssays, 21:326-332.[CrossRef][ISI]
Budd, G. E., and S. Jensen. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev, 75:253-295.
Buss, L. W. 1987. The evolution of individuality. Princeton University Press, Princeton.
Conway Morris, S. 1989. Early metazoans. Science Progress, Oxford, 73:81-99.
Conway Morris, S. 2000. The Cambrian "explosion": Slow-fuse or megatonnage? Proc. Nat. Acad. Sci. U.S.A, 97:4426-4429.
de Rosa, R., J. K. Grenier, T. Andreeva, C. E. Cook, A. Adoutte, M. Akam, S. B. Carroll, and G. Balavoine. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature, 399:772-776.[CrossRef][Medline]
Dewel, R. A. 2000. Colonial origin for Eumetazoa: Major morphological transitions and the origin of bilaterian complexity. J. Morphol, 243:35-74.[CrossRef][ISI][Medline]
Dzik, J. 1993. Early metazoan evolution and the meaning of its fossil record. In M. K. Hecht (ed.), Evolutionary biology 27, pp. 339–386. Plenum Press, New York.
Fedonkin, M. A., and B. M. Waggoner. 1997. The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature, 388:869-871.
Finnerty, J. R., and M. Q. Martindale. 1999. Ancient origins of axial patterning genes: Hox genes and ParaHox genes in the Cnidaria. Evol. Dev, 1:16-23.[Medline]
Gauchat, D., F. Mazet, C. Berney, M. Schummer, S. Kreger, J. Pawlowski, and B. Galliot. 2000. Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc. Nat. Acad. Sci. U.S.A, 97:4493-4498.
Gehling, J. G. 1991. The case for Ediacaran fossil roots to the metazoan tree. Mem. Geol. Soc. India, 20:181-224.
Gehling, J. G., G. M. Narbonne, and M. M. Anderson. 2000. The first named Ediacaran body fossil, Aspidella terranovica. Palaeontology, 43:427-456.[CrossRef][ISI]
Glaessner, M. F. 1984. The dawn of animal life. A biohistorical study. Cambridge University Press, Cambridge.
Holland, P. W. H. 1998. Major transitions in animal evolution: A developmental genetic perspective. Amer. Zool, 38:829-842.
Jackson, J. B. C., L. W. Buss, and R. E. Cook.(eds.) 1985. Population biology and evolution of clonal organisms. Yale University Press, New Haven.
Kourakis, M. J., and M. Q. Martindale. 2000. Combined-method phylogenetic analysis of Hox and ParaHox genes of the Metazoa. J. Exp. Zool. (Mol. Dev. Evol.), 288:175-191.
Martin, M. W., D. V. Grazhdankin, S. A. Bowring, D. A. A. Evans, M. A. Fedonkin, and J. L. Kirschvink. 2000. Age of Neoproterozoic bilatarian body and trace fossils, White Sea, Russia: Implications for metazoan evolution. Science, 288:841-845.[CrossRef][ISI][Medline]
Rieger, R. M., G. Haszprunar, and P. Schuchert. 1991. On the origin of the Bilateria: Traditional views and recent alternative concepts. In A. M. Simonetta and S. Conway Morris (eds.), The early evolution of Metazoa and the significance of problematic taxa, pp. 107–113. Clarendon Press, Oxford.
Seilacher, A. 1984. Late Precambrian and early Cambrian Metazoa: Preservational or real extinctions? In H. D. Holland and A. F. Trendal (eds.), Patterns of change in earth evolution, Dahlem Konferenzen, pp. 159–168. Springer-Verlag, Berlin.
Sibly, R. M., and P. Calow. 1986. Physiological ecology of animals: An evolutionary approach. Blackwell Scientific Publications, Oxford.
Simonetta, A. M., and S. Conway Morris.(eds.) 1991. The early evolution of Metazoa and the significance of problematic taxa. Clarendon Press, Oxford.
Stearns, S. C. 1982. The role of development in the evolution of life histories. In J. T. Bonner (ed.), Evolution and development, pp. 237–258. Springer-Verlag, Berlin.
Stearns, S. C. 1987. The evolution of sex and its consequences. Birkhäuser, Basel.
Valentine, J. W., D. Jablonski, and D. H. Erwin. 1999. Fossils, molecules and embryos: New perspectives on the Cambrian explosion. Development, 126:851-859.[Abstract]
Wainwright, S. A. 1988. Axis and circumference. Harvard University Press, Cambridge, Massachusetts.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||