Ontophyletics: Studying Evolution beyond the Genome

ONTOPHYLETICS: STUDYING EVOLUTION BEYOND THE GENOME MICHAELJ. KATZ* For an organism to evolve, its genome must change. However, the genome alone is not the organism. Organisms are the products ofdevelopmental sequences, ontogenies; and, for organisms with complex ontogenies , the developmental sequence itself can sometimes play a significant role in guiding evolution. In an ontogeny, the genome and the other preexisting structures of the egg and the sperm interact with each other and with the environment in a reproducible series of tissue, cell, and molecular transformations . As development proceeds, new patterns of cells and of molecules emerge as the products ofmany genes or as the products ofthe products of many genes. And, in this way, the manifest organism becomes distant from its genome. In this distance—in the ontongeny that intervenes between genome and phenotype—certain complex developmental mechanisms become midwives to phenotypes that are neither explicidy nor rigidly programmed in the genome. These complex developmental mechanisms also influence the evolutionary process, and their role in evolution is a central question in the field of ontophyletics. Cuvier's Problem Ontophyletics arose in response to an evolutionary dilemma. Normal ontogenies are usually built upon the extensive interactions among the products of genes. Enzymes produced by one gene remodel proteins produced by other genes, and specialized cells, which express different Most of the ideas presented here evolved through extensive conversations with R. J. Lasek, who coined the term "ontophyletics." His constructive comments led to significant improvement in this manuscript. S. J. Gould introduced the author to Cuvier's Problem. This research was supported by grants from NIH and NSF. This essay was submitted in the first Dwight J. Ingle Memorial Young Writers' competition for authors under 35. *Department of Anatomy, Case Western Reserve University, Cleveland, Ohio 44106.© 1983 by The University of Chicago. AU rights reserved. 0031-5982/83/2602-0329$01.00 Perspectives in Biology and Medicine, 26, 2 · Winter 1983 | 323 genes, form cooperative tissues. These cooperative interactions depend on the appropriate matching between cells and between molecules, and much ofontogeny consists ofthe development ofappropriately matched populations of cells and of molecules. How can such appropriate matching be maintained after genomic changes? In other words, how can viable evolutionary changes occur in any but the most independent genes or the most mosaic ontogenies? I have stated this dilemma in contemporary terms, but the basic question predates proteins and genes—it even predates Darwin. This evolutionary dilemma was first set forth in the early 1800s by the antievolutionist Georges Cuvier [I]. Cuvier repeatedly pointed out that all organisms are tightly integrated wholes. He wrote: "Every organized individual forms an entire system of its own, all parts of which mutually correspond and concur to produce a certain definite purpose, by reciprocal reaction or by combining towards the same end. Hence none of these separate parts can change their forms without a corresponding change on the other parts ofthe same animal . . ." [2, p. 90]. Recognizing this fact, Cuvier asked how any well-integrated organism could ever evolve. To preserve the necessary integration, most evolutionary steps would require a great many diverse yet coordinated changes. But how could aU the appropriate changes come about (not just once, but time after time) to account for all the steps in an evolutionary scheme ofUfe? Cuvier could not find mechanisms that would lead to diverse yet coordinated changes, and so he was forced to deny the existence ofevolution. Cuvier was an insightful biologist. The founder of comparative anatomy, Cuvier had a firsthand detailed knowledge of many different organisms, and his antievolution stance was a reaction to certain nonbiological statements of contemporary evolutionists such as Lamarck. Cuvier knew that organisms do not fill a smoothly graded continuum of varieties, as Lamarck impUed. Nature is quantal, not graded, and most organisms can be arranged into separate classes of distinct wellintegrated body plans. Cuvier argued that the fundamental problem faced by any evolutionary theory was how one well-integrated body plan could .possibly evolve into another entirely different yet still wellintegrated body plan. Cuvier could not offer an alternative theory that unified biology as the evolutionary theory did, and with Darwin's Origin of Species evolutionary theory became well estabUshed. Nonetheless...