Why Developmental Biology is Important to Paleontology
Abstract.- Paleontologists deal with the morphologies of ancient organisms, usually recorded only as skeletal remains, alas, or even only as trace fossils. Still, the patterns of appearance, change, and disappearance of morphologically defined taxa not only indicate the historical pathways of evolution, but establish requirements for evolutionary processes: the processes must be capable of producing the recorded histories. It is natural enough for paleontologists to believe that evolutionary hypotheses that cannot account for the fossil record are flawed. On the other hand, when interpretations of fossil patterns violate established evolutionary principles, there is certainly reason to restudy and reinterpret the patterns. In the past, fossil patterns have been used to support such notions as vitalism, orthogenesis, and the biogenetic law of recapitulation, ideas that have proven incompatible with biological facts. Clearly, viable hypotheses to account for patterns of morphological change must be able to satisfy the findings of many fields.
Of course disputes abound within all fields, and it is commonly not possible for workers in one field to evaluate properly the status of ideas that are under dispute in other fields. For paleontologists, genetics affords excellent examples. During the early decades of this century, workers in transmission genetics tended to downplay the importance of developmental genetics, especially when it came to evolution, despite important research that suggested there was more to the story (e. g., Harwood 1993; Nyhart 1995). When genetics became involved in developing an "evolutionary synthesis," it was Dobzhansky (1937), Stebbins (1950), and others with experience in morphology who largely fashioned the genetic contributions (see Mayr 1980). Many transmission geneticists simply argued for the sufficiency of an interplay of an expansion of Mendelian inheritance with selection to explain the genetics of evolution ("microevolution"), and many paleontologists followed suit. Even G. G. Simpson (my personal paleontological hero) largely took that tack (1944, 1953).
In spite of Simpson's heroics, the abruptness with which major morphological innovations appear in the fossil record suggests that there might be evolutionary modes beyond classic microevolutionary change. If so, the explanation seems likely to lie in the relation between the transmission of traits and the development of morphology; the complexity of the developmental process has hindered advances in that area until relatively recently. However, the rise of molecular developmental biology is revolutionizing the field of developmental genetics, and the transmission of complex morphologies from organs to whole body plans, not as collections of atomistic alleles but as integrated systems, can finally be brought under study. To paleontologists interested in the evolution of morphology, these studies are of the highest significance, regardless of how accurate the fossil record of morphological innovation turns out to be.
In The Shape of Life, Rudy Raff has written a book that presents major aspects of developmental biology in an evolutionary context, at a level that is accessible to graduate students in paleontology, and indeed to undergraduates who have had a strong introduction to biology. The subtitle is "Genes, Development, and the Evolution of Animal Form," which pretty much indicates the major topics. Animal phyla are briefly defined and the nature of their early fossil records during the Neoproterozoic and the Cambrian is reviewed. In order to evaluate this record better, and particularly to understand the pathways of developmental evolution, it is necessary to understand the branching pattern of the tree of metazoan life. And in fact, the first full-blown attempts to build a tree of the major animal phyla from 18S ribosomal RNA evidence emerged from Raff's laboratory, and his account of the rationale, the methods, the results, and the difficulties in molecular phylogenetics is skillfully presented. Raff then goes on to describe what is known of the developmental controls that mediate body plan development, including an account of the genes, such as the Hox cluster, that are so intimately concerned with differentiation of the adult body plan. This field is moving very fast indeed; for example, research on the Hox cluster in Amphioxus has already overturned early accounts.
Raff stresses the concept of a phylotypic developmental stage, at which the genes that mediate the architecture of the basic body plan are essentially all expressed (see Slack et al. 1993). Earlier stages, as embryos or larvae, may vary greatly among members of a phylum, while later stages clearly vary significantly among different classes, orders, and other taxa, but at the phylotypic stage the different members of a phylum are most similar. Raff discusses observations and experiments (much his own) with direct and indirect development in closely related echinoids, and other work of this sort, and explores the sorts of constraints that might preserve a phylotypic stage despite such important variations in early development. And finally, he examines the problems that lie ahead in unraveling the evolution of novelties and suggests directions for future work. All this is rich in detail, with explorations of many byways in development and evolution.
The style, while not breezy, is quite personal, with sections devoted to tales of high adventure (with scientific implications to be sure) and to Raff's own involvement in everything from attending conferences to involvement in difficult but successful research projects. Raff writes well and I quite liked this approach, which helped rescue the scientific findings from the formalities of abstraction, and lent them an immediacy and relevancy that they certainly deserve. On the other hand there are no bibliographic citations in the text, although workers are mentioned as their researches come up, and there is no author index, although there is a bibliography that lists the works that are drawn on. This lack of citation machinery furthers the personalized feel of the writing, but at the same time it distances the reader from the primary literature and reduces the ability to evaluate critically the notions that are being propounded, which is unfortunate.
It is unusual to find significant space devoted to the fossil record in a book that is essentially about development, and Raff's most praiseworthy inclusion of fossil evidence indicates his understanding that paleontology and developmental biology have something to offer each other. The evolution of novel morphologies, which are abundantly documented by the fossil record, must be underlain by the sorts of developmental evolution that Raff describes, and It seems likely that, if the many rather abrupt appearances of novel morphologies are real, the explanations are to be found in these processes. Thus I applaud the fossil material wholeheartedly but must also report that it contains numbers of minor errors and omissions, the sort that will make most paleontologists wince a bit. The accounts of the fossils seem to have been drawn chiefly from secondary sources, and without detailed citations the original work cannot be followed up. Happily, these minor problems do not detract from the general thrust of the message. Paleontologists will know better than to be misled, and should benefit enormously from the fine introduction to developmental evolution that Raff has provided here. Armed with the perspectives of this book, paleontologists should be stimulated to read further, perhaps more technical accounts such as Scott Gilbert's Developmental Biology, and to delve into the technical reviews and primary literature of this fascinating field. Developmental biology is in so many ways concerned with the same problems that face paleontologists: the problems of the evolution of organic form. I heartily recommend The Shape of Life to all.
James W. Valentine, Museum of Paleontology and Department of Integrative Biology, University of California, Berkeley, California 94720