Rudolf Raff is recognized as a pioneer in evolutionary developmental biology. In their 1983 book, Embryos, Genes, and Evolution, Raff and co-author Thomas Kaufman proposed a synthesis of developmental and evolutionary biology. In The Shape of Life, Raff analyzes the rise of this new experimental discipline and lays out new research questions, hypotheses, and approaches to guide its development.

Raff uses the evolution of animal body plans to exemplify the interplay between developmental mechanisms and evolutionary patterns. Animal body plans emerged half a billion years ago. Evolution within these body plans during this span of time has resulted in the tremendous diversity of living animal forms.

Raff argues for an integrated approach to the study of the intertwined roles of development and evolution involving phylogenetic, comparative, and functional biology. This new synthesis will interest not only scientists working in these areas, but also paleontologists, zoologists, morphologists, molecular biologists, and geneticists.

THE SHAPE OF LIFE

Genes, Development, and the Evolution of Animal FormBy Rudolf A. Raff

THE UNIVERSITY OF CHICAGO PRESS

Copyright © 1996 The University of Chicago
All right reserved.
ISBN: 978-0-226-70265-0

Contents

Preface......................................................................xiiiAcknowledgments..............................................................xxi1 Over the Ice for Ontogeny and Phylogeny....................................12 Metazoan Phyla and Body Plans..............................................303 Deep Time and Metazoan Origins.............................................634 Molecular Phylogeny: Dissecting the Metazoan Radiation.....................1035 Recovering Data from the Past..............................................1426 The Developmental Basis of Body Plans......................................1737 Building Similar Animals in Different Ways.................................2118 It's Not All Heterochrony..................................................2559 Developmental Constraints..................................................29210 Modularity, Dissociation, and Co-option...................................32111 Opportunistic Genomes.....................................................36212 Evolving New Body Plans...................................................397References...................................................................435Index........................................................................493

Chapter One

Over the Ice for Ontogeny and Phylogeny

In the strait of Magellan, looking due southward from Port Famine, the distant channels between the mountains appeared from their gloominess to lead beyond the confines of the world.

Charles Darwin, Voyage of the Beagle

THE WORST JOURNEY IN THE WORLD

As a young man, Apsley Cherry-Garrard spent two and one-half years as an unpaid assistant zoologist on Robert Falcon Scott's fatal 1911 expedition to Antarctica and the South Pole, then returned to England in time to see the start of World War I. He survived military service in Flanders, and found the time to publish in 1922 one of the most extraordinary accounts of polar exploration ever written, The Worst Journey in the World. There he vividly and movingly tells of the tragic fates of Scott and his polar party, but within that grander tragedy he records the staggering difficulties of one of the strangest trips ever undertaken, his own appalling winter journey with ornithologist Edward A. Wilson and Royal Navy lieutenant H. R. Bowers to Cape Crozier to collect the eggs of the emperor penguin. The same zeal for scientific discovery that lured Darwin and so many other great scientific voyagers drew Cherry-Garrard and the other members of the party on a journey of scientific exploration that they barely survived. Cherry-Garrard's idealism comes through in the words he wrote many years later: "We traveled for Science. These three small embryos from Cape Crozier, that weight of fossils from Buckley Island, and that mass of material, less spectacular, but gathered just as carefully hour by hour in wind and drift, darkness, and cold, were striven for in order that the world may have a little more knowledge, that it may build on what it knows instead of on what it thinks." Bowers and Wilson were later to die with Scott on their return from the South Pole. Their passion for science may have contributed to their deaths. They had collected several kilograms of fossil plants from some of the few exposed rocks of the Antarctic continent at Beardmore Glacier in the Transantarctic Mountains. Despite their exhaustion, Scott's South Pole party attempted to return with the specimens the three hundred-odd miles from Beardmore Glacier to their base camp on Ross Island. The fossils were found on their sled at their final camp where they died in a blizzard. The fossils were recovered by the rescue party, and much later in the century were to lead to the discovery of fossils of Triassic mammal-like reptiles in Antarctica. The remains of these animals, so akin to the contemporary mammal-like reptiles of Africa, established that about 250 million years ago Antarctica, along with Africa and Australia, made up the southern part of the supercontinent of Pangaea.

The main goal of Scott's expedition was to be the first to reach the South Pole. Nevertheless, in Scott's mind, his expedition was primarily a scientific journey of exploration, not merely a race with Roald Amundsen's Norwegian polar party. Wilson's satellite expedition to Cape Crozier was driven by the desire to test an evolutionary hypothesis about embryonic development and its relationship to evolutionary history. The reasons underlying the six-weeklong sled journey to a penguin rookery in the continuous dark of the Antarctic winter seem extraordinary, but they are not so different from the foundations of many other expeditions dispatched across the planet and into space on the basis of what later were shown to be very shaky theoretical concepts.

Darwin's most forceful adherent was the German zoologist Ernst Haeckel, who became the most prominent late-nineteenth-century evolutionary theorist. Haeckel's achievements included the coining of numerous scientific terms (including such enduring favorites as ecology, phylogeny, and heterochrony), the prediction of the discovery of a fossil link between apes and humans (he called it Pithecanthropus), and the inauguration of a passionate quest for phylogenetic trees. In 1866 he propounded the famous and overwhelmingly influential biogenetic law, which states that ontogeny (the development of the individual) results from phylogeny (the evolutionary history of the lineage). Haeckel's mechanism of evolution required that new forms appear as a result of the addition of new terminal stages to the ancestral ontogeny. Thus, all animals should recapitulate their phylogenies in an abbreviated form during development, and developmental stages should reveal those histories. In 1911 Haeckel's ideas still held powerful sway in the minds of zoologists, a vision potent enough to send men on a desperate journey through the Antarctic night. It was Wilson's idea that the emperor penguin is the most primitive living bird, an evolutionary relict, a creature pushed to the very farthest reaches of the south polar regions by competition with more recently evolved and more advanced groups of birds spilling out of Eurasia. In the first decades of the twentieth century, Eurasia was thought by zoologists to be the center of many evolutionary radiations, a cauldron of Darwinian competition. It was thought that humanity originated there as well. Less fit species either became extinct or sought refuge in peripheral parts of the world not reached by their superior competitors.

The winter trip to the penguin rookery was aimed at preserving eggs in fixative and bringing them back to England for study. Wilson thought that if the trip took place early enough in the breeding season, various early developmental stages would be represented in the sampled eggs. Because in Wilson's scenario the emperor penguin is a primitive relict, its embryos were expected to recapitulate the reptile-to-bird transition. As Cherry-Garrard put it, "it is because the Emperor is probably the most primitive bird in existence that the working out of his embryology is so important. The embryo shows remains of the development of an animal in former ages and former states; it recapitulates its former lives. The embryo of an Emperor may prove the missing link between birds and the reptiles from which birds have sprung." This is a clear expression of Haeckel's dogma. Modern bird embryos do not reveal much about their reptilian ancestry. But, in Haeckelian recapitulation theory, it would be expected that with addition of more modified late stages in advanced birds, some of the early evolutionary stages would become so compressed as to effectively vanish. Thus, Wilson wanted to look at what he thought was the most primitive bird, because it would have undergone less modification of its development, and still might recapitulate some reptilian stages.

The trip was executed with awesome persistence in the face of the unending darkness, the killing cold, and the broken and barely visible terrain. Each man pulled a sled loaded at the start of the trip with 250 pounds of food and supplies. Condensation from their breath froze in clothing and sleeping bags, converting these items into a reluctant frozen armor that had to be forced on with help. The extreme cold prevented the snow from melting beneath the sled runners and forming a lubricating film of water. The result was a pull over snow that had the friction of sand. Cherry-Garrard's account of the daily routine is painful: "That day we made 3¼ miles, and traveled 10 miles to do it. The temperature was -66° when we camped, and we were already pretty badly iced up.... For me it was a very bad night: a succession of shivering fits which I was quite unable to stop." The physical toll mounted. Cherry-Garrard records, "I don't know why our tongues never got frozen, but all my teeth, the nerves of which had been killed, split to pieces."

"And then we heard the Emperors calling."

After nineteen days, they reached the rookery at Cape Crozier. Penguins stood with eggs tucked up onto their feet and under their breast feathers. It required a difficult climb down over the 200-foot ice cliffs to get to the rookery, and only five eggs could be collected from the frightened birds. A blizzard lasting several days prevented any further attempts. In the exertions of returning to camp, two of the eggs were broken; the three survivors were preserved and ultimately returned to Britain.

A thorough analysis was finally published by the ornithologist Cosser Ewart in 1921. Ironically, when the eggs were finally studied, the embryos so painfully recovered were found to be fairly late in development. Wilson's hope of examining early stages was not to be fulfilled. Thus, the test made of recapitulation was limited to seeing whether scales arise before feather primordia. That would be expected in a strict recapitulation in the development of a primitive bird because scales are the homologues of feathers and are their evolutionary precursors. The homology of scales and feathers is supported by the existence of mutations in chickens in which the scales that normally cover the legs are converted to feathers. However, Ewart found that, as in other birds, the emperor penguin's feather primordia form prior to the scale primordia. It has since been shown that penguins have a good fossil record dating back over 40 million years and evolved deep in the Southern Hemisphere from a flying seabird ancestor. Wilson's driving idea became an irrelevance, based both on a misreading of the relationship of biogeography to evolution and on a misplaced faith in an oversimplistic theory of the evolutionary meaning of development.

OLD ROOTS AND TANGLED BRANCHES

Many of the ideas we cherish as novel have origins that predate us by embarrassingly long times. Current studies of the relationship between development and evolution also have a long and complex evolutionary history. To place a new discipline of evolutionary developmental biology in its proper context, we must trace that history. What I attempt to do in this chapter is to show that this discipline has deep roots in biology. These roots have nourished a complex tangle of ideas. At times the fusion of developmental biology and evolutionary biology has been central to a generation's understanding of evolution. At other times only a few biologists have had any interest in the subject, and the two disciplines have each advanced along their own internally driven paths with scarcely a polite glance at each other. The story is not a neat one. There has been a tangle of ideas that have derived from quite disparate disciplines.

History is not merely a record of the dead past. The questions and problems that we will deal with in this book in many cases arose long ago, but remain unresolved. They merely appear in new guises and demand new approaches. Furthermore, the paths traveled during the past century by the disciplines that we are trying to fuse have created domains of thought that are in substantial ways different and not easily melded. The invention of new tools and the discovery by developmental geneticists of deep commonalities in the genetic regulatory mechanisms underlying animal development have inevitably led to the experimental study of the evolution of development. However, to be fully meaningful, such a new discipline must truly fuse older disciplines, not merely attempt to impose a dataset derived from developmental or molecular biology upon a superficial idea of evolution.

RECAPITULATION, TRANSFORMATION, AND VON BAER'S LAWS

The idea of developmental recapitulation as a guide to evolutionary history that sent Cherry-Garrard's party over the ice was an outgrowth of one of the grandest synthetic concepts of biology. This idea was at first pervasive in driving research and later soundly derided. For all of the problems in its application, however, recapitulation in part reflects very real phenomena in the evolution of developmental patterns. Pre-Darwinian comparative anatomists in the early nineteenth century noted a very striking thing: in their development, the embryos of higher organisms appeared to pass through, or recapitulate, the features seen in the adults of related lower organisms. Many of the adherents of a literal recapitulation saw the animal kingdom as a linear progression of various invertebrate groups culminating in the vertebrates and humans. As elaborated by Louis Agassiz in 1849, this comparative anatomical discovery could be given a time dimension as well by examination of the fossil record. Agassiz suggested that a threefold parallelism is evident as the embryo of a higher animal passes through its developmental stages. In many cases a series of developmental stages resembles both the adults in a series of more primitive related forms and the progression of fossil representatives of the group through geologic time. For example, the juveniles of modern bony fishes, Agassiz's favorite animals, initially develop tails similar to those characteristic of adults of primitive fossil species, and only later develop modern-style tails. Some biologists saw in this phenomenon support for "transformation," the pre-Darwinian term for evolution. Not Agassiz. To him, the threefold parallelism did not reflect any transformation between forms, but an underlying "plan designed by an intelligent creator." Although he had revolutionized geology through his discovery of the Ice Age and later founded the Museum of Comparative Zoology at Harvard, he stubbornly, and to modern eyes perversely, opposed evolution throughout his entire life. In an 1867 letter to a colleague (cited by Winsor), he wrote of Darwinism, "I trust to outlive this mania." He didn't.

The embryological supports for parallelisms between developmental stages and levels of animal complexity were often speculations based on poorly interpreted data. There are some notorious examples. The famous French anatomist Geoffroy Saint-Hilaire homologized the internal skeleton of vertebrates with the exoskeleton of arthropods (see Appel). As he summed it up, "every animal lives within or without its vertebral column." His contemporary Etienne Serres considered human teratological monsters to be arrested at the stages of adults of lower forms. Thus a headless human fetus reflected the clam stage, since these mollusks seemed to be the highest headless animals. Although evolutionary ideas colored the ideas of the biologists of the transcendental school, the concept of linear recapitulation harked back to the much more ancient concept of the Great Chain of Being propounded by Aristotle and later sanctified by the Church because it illustrated the plenitude of God's creation. In the great chain or ladder, all possible living creatures had been created by God in order, from the most simple, such as plants, through various invertebrates, lower vertebrates and higher, man, and finally angels and other supernatural beings. Superficially, the idea looks evolutionary, but it was not. The scheme was static, not transformational. No one climbed this ladder except embryos.

In 1828 the great embryologist Karl Ernst von Baer carried out the investigations of vertebrate development that led to his famous empirical "laws," which were intended to deal a stunning blow to loose theorizing on the nature of development. Von Baer's observations showed that there is no strict recapitulation of the development of a more primitive form by the embryo of a more advanced one. Instead, organisms diverge from one another in development. The embryos of higher forms do not duplicate the adults of more primitive relatives, but in their stages of development they do resemble the stages of development of the embryos of related lower forms. Von Baer intended his "laws" to make the theory of recapitulation untenable. His results showed that fancied resemblances across phyla, such as those proposed by Serres, were unfounded. The body plans revealed by development were clearly specific to each of the great "embranchements" defined in 1812 by Georges Cuvier, the father of comparative anatomy. These great branches of the animal kingdom, radiates (coelenterates and echinoderms), mollusks, articulates (insects, crustaceans, and annelids), and vertebrates, were each characterized by unique and distinct body plans. There was not one great chain, but four branches. Cuvier's definitions of these embranchements were based on characteristic modes of organization of the nervous system, and they have a rough correspondence to the phyla we currently recognize. Cuvier considered the nervous system to be the primary functional system, and thus its organization the critical feature of each body plan. Like the fundamentally different developmental pathways defined by von Baer, the embranchements of Cuvier argued against evolution. For Cuvier it was not just that the embranchements were different in morphology; integrated function also was crucial. Cuvier believed that the radically different organizations of the four embranchements could not change from one to another without a fatal loss of integrated function during the transition. This argument is still a forceful one.

I do not want to leave behind a caricature of the events I have outlined above. Words like "notorious" and "loose theorizing" are highly colored and imply that the activities of the transcendentalist biologists were somehow silly or irrelevant because they did not correspond to our view of things. Nothing could be further from the truth. The first quarter of the nineteenth century was a time of roiling intellectual ferment and methodological innovation in biology. We look at formal portraits of remote scientists like Cuvier with his high-necked brocade jacket and medals, and too easily forget that all the petty jealousies, academic politics, and power struggles, as well as the grander passions of scientists for their viewpoints, existed then as now.

(Continues...)

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