Looking at the Origins of Body Plans

As a child, Rudolf Raff found the living things he could observe in the woods behind his parents' home fascinating. He marveled at the diversity of forms he observed. Salamanders, toads, worms, beetles, spiders, and moths were each distinct living things. "Why were earthworms so different from the insects and salamanders that shared the woods with them?" Raff wondered.

Developmental biology, Raff's specialty, addresses the question of how life develops in embryo. The process of embryo development is something akin to a miracle: a single, fertilized cell develops into an organism with millions of specialized cells, all working together. The regulation of these developmental events is currently a major area of biological research, which seeks to understand the genetic and molecular controls that produce a complicated organism.

Developmental biology has in recent years acquired the powerful tools of molecular biology and genetics. By examining the DNA and RNA proteins in the genetic material of cells, scientists can study the regulators of development at the cellular level. This has led to a better understanding of a "body plan": how a fertilized cell organizes its cleavage and development into a complex organism.

Development produces the body shape of the individual; evolution, in parallel, produces the body plans of the animal kingdom. "Most people," says Raff, "can grasp that we are related to monkeys, that we have a common ancestor. Tell them that we are also related to spiders--if you go back far enough, about 600 million years--and the idea just seems too bizarre for many people. But it's true."

Spiders and humans seem so different because each has evolved a distinct body plan. Scientists classify organisms sharing a common anatomical plan together in a phylum. For example, humans belong to the phylum Chordata, spiders to the phylum Arthropoda. Until recently, evolutionary biologists had to depend on observations of morphology (body features) to determine relations among phyla, a strategy that did not always give a clear idea of the actual evolutionary path. The presence of some body feature--be it arms and feet, an external shell, or segmentation--may indicate genetic relationship to other animals with that same feature. But it may also be an independent adaptation to the environment, for if particular features help some creatures to flourish, the same features are likely to be useful to other creatures as well.

Raff and others interested in the evolution of body plans have thus used the tools of molecular biology to clarify relationships among phyla and within phyla. The genetic instructions carried in DNA operate at the level of the cell to regulate development, but they also are a record of the evolutionary development of the organism.

Evolutionary biology and developmental biology were once closely linked. At the end of the last century, the scientist Ernst Haeckel coined the phrase "ontogeny recapitulates phylogeny," and countless biology students have memorized these words since then. Scholars found that Haeckel's observation was useful to a point: the embryo of advanced life forms does, in its developmental stages, present a broad parallel to the evolution of species from single-cell protozoa to more and more organized units of specialized cells. Over the past ninety years, however, the two fields, developmental biology and evolutionary biology, went their separate ways. Raff's work brings them together again.

Raff and his colleagues have shown how the sequences of ribosomal DNA in cells of animals can be compared to one another to determine the closeness of the genetic relationship. One example is DNA sequencing with arthropods.

The arthropods (including insects, spiders, and crustaceans) are the most successful of all phyla and make up three quarters of all living species in existence. In absolute numbers, also, they are far more numerous than, for example, mammals. There has long been controversy about the origin of arthropods. Did they arise from a number of different phyla through convergence? Or did all anthropods arise from a single ancestral line? Studies of ribosomal DNA sequences in the cells of arthropods indicate to Raff and his colleagues that all arthropods have a single ancestral line and that both arthropods and annelids (e.g., earthworms, tapeworms), and a member of the phyla, including molluscs, arose from a common ancestor. That ancestor probably had a wormlike body and segmentation; the arthropods subsequently evolved the hard exoskeletons and jointed appendages that typify their phylum.

Going back further in evolutionary time, Raff and collaborators have studied the findings of DNA sequencing for a number of animal phyla. Results from Raff's laboratory, and those of other molecular evolutionists, have allowed us to see a more complete picture of the origins and divergences of the animal phyla. DNA sequencing can also shed light on those areas of evolution for which the fossil record is scarce or absent. DNA sequencing has revealed that animals have their roots in single-celled organisms. The three basic groupings of life are plants, fungi, and animals; genetic sequencing indicates that animals and fungi share a sister relationship, and the two are more distantly related to plants.

But Raff also recognizes that DNA sequencing is a complement to morphology studies, not a substitute, and that its methodology is not fully developed. "The information you get has to be weighed against knowledge from other sources," he cautions. Only when the information obtained from molecular analysis is concordant with other data can strong inferences be obtained.

It is not just the application of DNA sequencing in molecular biology that Raff advocates for evolutionary studies. He also believes that developmental biology informs evolutionists about the processes they study. In an essay on the evolution of two types of sea urchins, Raff points out that well-known developmental processes "may account for many of the major evolutionary differences in cell lineage and axis formation." Raff studied two types of sea urchins with almost identical adult morphologies. The crucial difference between the two lay in their development from embryo to adult. One type of sea urchin has conserved the ancestral pattern of indirect development from embryo through a feeding larval stage. Ultimately, metamorphosis produces a juvenile stage that grows to adulthood. The other sea urchin type has a larger egg that develops directly and quickly into the juvenile stage. The larval stage in this second, direct-developing type, has been bypassed. Here was a case of extensive genetic remodelling in early development, even though the final outcome--the adult--was virtually the same in morphology and habits as the indirect-developer .

Raff found that one key to this change in development was the suppression of the older pattern of development of a larval skeleton and larval feeding structures (mouth and gut). But it was not only the suppression of older patterns that accounted for subsequent direct development. The entire program of body development had been remodeled, with resulting changes in the fate of cells in interaction with one another.

The astonishing range of changes in embryonic development of the direct-developing sea urchin can, Raff argues, provide a model for the rapid evolution of forms in the distant past. This model may help to explain how so many forms developed during the Cambrian radiation, an early phase of the fossil record dated to 540 million years ago. The sea urchin model informs both developmental biologists and evolutionary biologists. Developmentalists have primarily viewed development as a mechanistic process that, by its nature, predetermines adult morphology; evolutionists have focused on genetic variation in development and have seen development as a process that can constrain or shape evolution. Raff has shown through his study of sea urchin development that there is mechanistic constraint in the middle of development, but that great variation can occur in both early development and in the final stages of development. Thus both conservation and variation are part of the evolution of development, but conservation is especially pronounced in development of the body plan itself.

As a leader in forming this fertile hybrid field of evolutionary developmental biology, Raff discusses the ultimate goal of his research. "Even if the purpose is to inform us about our own origins, developmental biologists work with other organisms to get those answers. Humans have long life spans and aren't amenable to laboratory observation. In our work we use species that are abundant and have short life spans, like fruit flies and sea urchins."

Raff's plans for the future include continuing to research embryo development, to act as an advocate for the hybrid field of evolutionary developmental biology, and to further hone molecular analysis tools, like DNA sequencing. To promote this last goal, Raff founded the Indiana Institute for Molecular and Cellular Biology eleven years ago, and he continues to serve as its director [see sidebar]. He has distilled his ideas on evolution and development into a book, The Shape of Life, to be published next year by the University of Chicago Press. This work is for graduate students and scientists, but Raff has another book in the planning stage: a work for a general audience on the use of DNA to explore deep time. Raff continues to enjoy the questions as much as the answers.

--William Rozycki