UNCORRECTED PAGE PROOFS Animal Architecture 3 and the Bauplan Concept The business of animals is to stay alive until they reproduce themselves, and . the business of zoologists is to try to understand how they do it. E. J. W. Barrington, Invertebrate Structure and Function, 1967 he German language includes a wonderful word that expresses the essence of animal architecture: Bauplan (pl. Baupläne); we will use the Anglicized spelling, bauplan (pl. bauplans). The word means, literally, “a Tstructural plan or design,” but a direct translation is not entirely adequate. An an- imal’s bauplan is, in part, its “body plan,” but it is more than that. The concept of a bauplan captures in a single word the essence of structural range and architec- tural limits, as well as the functional aspects of a design (Box 3A). If an organism is to “work,” all of its body components must be both structurally and functional- ly compatible. The entire organism encompasses a definable bauplan, and the specific organ systems themselves also encompass describable bauplans; in both cases the structural and functional components of the particular plan establish both capabilities and limits. Thus, the bauplan determines the major constraints that operate at both the organismic and the organ system levels. The diversity of form in the biological world is dazzling, yet there are real lim- its to what may be successfully molded by evolutionary processes. All animals must accomplish certain basic tasks in order to survive and reproduce. They must acquire, digest, and metabolize food and distribute its usable products through- out their bodies. They must obtain oxygen for cellular respiration, while at the same time ridding themselves of metabolic wastes and undigested materials. The strategies employed by animals to maintain life are extremely varied, but they rest upon relatively few biological, physical, and chemical principles. Within the constraints imposed by particular bauplans, animals have a limited number of options available to accomplish life’s tasks. For this reason a few recurring funda- mental themes become apparent. This chapter is a general review of these themes: the structural/functional aspects of invertebrate bauplans and the basic survival 41 42 CHAPTER THREEUNCORRECTED PAGE PROOFS BOX 3A The Bauplan and Related Concepts Stability of organismal morphology is a standard phenotype in spite of ge- For example, we now know that much a deep-seated notion that dates at netic or environmental disturbances. of an animal’s initial embryogeny is least from the eighteenth century; the The concept can be viewed at the under maternal cytoplasmic control idea of a limited number of plans, genomic or organismal level, or even rather genomic control. However, at types, or archetypes of animal forms is at a character-by-character level. The some point early in embryogenesis, thus an old one. Richard Owen intro- more highly canalized a character the the zygote’s parental (nuclear) duced the term archetype in 1848 to less it will vary among individuals, and genome takes primary control of de- represent a model organism, or the characters that define bauplans are velopment. Recent work suggests that sum of the features shared by a group highly canalized. The preservation of this may be one of several pivotal of related organisms. The concept of Hox gene function across phyla is a points in the control of animal ontoge- the embryological archetype, and the good example of developmental ny—occasions that demarcate the fixa- fact that adults are nothing more than canalization. In fact, we are beginning tion of bauplans. The point at which the accumulation of features added to realize that many of the basic body the zygotic genome takes over control during their development, was formal- patterns that evolved during the Pre- of embryogenesis has been referred to ized by Karl von Baer and Ernst cambrian/Cambrian origins of animal by several names, but perhaps the Haeckel in the second half of the nine- phyla represent the outcomes of con- most fitting term in the literature is the teenth century. Today this concept has served genes and developmental zootypic stage. It may be here that grown into the notion of conserved plans. the Hox genes establish the most body plans, or Baupläne (bauplans, in The characteristics of an organism’s basic, or primary, animal body pattern- the Anglicized form used in this book). bauplan are not the same thing as its ing (e.g., the anterior–posterior axis The concept speaks to a stability in phylogenetically unique features, or and dorsal–ventral surfaces). form that maintains itself through evo- synapomorphies. Instead, bauplans At a later stage of embryogenesis lutionary time and phylogenetic diver- must be viewed as nested sets of con- another critical point is reached, which gence. served body plans, as would be pre- has been called the phylotypic (= The term Bauplan (German for dicted within an ancestor–descendant phyletic) stage. The phylotype theoreti- “ground plan” or “blueprint”) was in- hierarchical system such as animal cally represents the stage when the troduced as a technical term in zoolo- phylogenesis. For example, snakes genes responsible for secondary pat- gy in 1945 by the embryologist- possess a bauplan that differs from the terning of a body plan are first fully ex- turned-philosopher Joseph Henry bauplans of lizards, turtles, or croco- pressed and the adult morphogenetic Woodger. More recently, Niles diles—yet each shares the reptilian fields are positioned. This juncture is Eldredge (1989) discussed the bauplan bauplan. Reptiles, birds, and mammals not well understood. Anderson (1973) as the common structural plan within each have individual bauplan but identified the blastula as the phylotyp- a monophyletic taxon; Valentine share the vertebrate bauplan. Thus, ic stage for the annelids and arthro- (1986) distinguished bauplans as as- bauplans consist of a mix of ancestral pods, whereas Sander (1976, 1983) semblages of homologous architectur- and derived characters. To understand identified the germ band stage (a 20- al and structural features distinguish- their origin requires knowledge of segmented larval stage with head, ing phyla and classes; and Gould adult, larval, and embryonic phases of thorax, and abdomen already delin- (1977, 1980, 1992) spoke of structural the life cycle. eated and segmented) as the phylo- constraints leading to fundamental Woodger explicitly argued, as had typic stage of insects. Cohen (1977, ground plans of anatomy. And, in his von Baer, that the most basic struc- 1979), on the other hand, distin- review of the reunion of developmen- tures defining the bauplan develop guished phylotypic larvae (the tro- tal and evolutionary biology, Atkinson early in embryonic life. Consequently, chophore of annelids, for instance) (1992) claimed that “the single most deviations early in development would from adaptive larvae. Phylotypic stage critical concept of the reunion is that have much more drastic consequences larvae have a simple morphology de- of the bauplan.” for morphology than deviations later termined more by developmental (ge- The concept of the bauplan ex- in development. Mechanisms that es- netic) programs than by physiological presses both a notion of morphologi- tablish bauplans buffer development requirements. cal stability and the fact that some as- against environmental and genetic The phylotypic stage is usually pects of embryonic and/or adult perturbations. They constrain develop- thought of as the stage at which em- morphology are more free to vary ment. Ernst Mayr repeatedly drew at- bryos within a phylum show the great- than are others. That is, some stages of tention to the importance of such con- est level of morphological similarity. development are more constrained straints, specifically in relation to Beyond this stage, the zygotic genome than others. The most striking evi- bauplans, conserved morphological begins moving embryos down the in- dence of developmental constraints is features, and the taxonomic features dividual tracks of the various lineages. the simple fact that, despite the great used in classification. Heterochrony In other words, early developmental variety of animals, there are relatively (see Chapter 4) may be one powerful stages of closely related taxa converge few basic types of animal body plans. force that can alter or overcome the on a phylotype in the course of their Developmental canalization, inertia of bauplans. ontogeny, only to diverge again as the sometimes called developmental buffer- The field of molecular evolutionary adult form unfolds. ing or genetic homeostasis, is a form of developmental biology is just emerg- Thus it seems likely that there are constraint that channels ontogeny into ing, but already its discoveries are several fundamental levels of body restricted sets of pathways that lead to shedding new light on these old ideas. patterning during ontogeny, and ANIMAL ARCHITECTURE AND THE BAUPLAN CONCEPT 43 UNCORRECTED PAGE PROOFS closely related taxa share critical junc- 1. Structural constraints (e.g., con- 6. Functional constraints (e.g., the tures of this process in ways that hear- straints imposed by the limita- interconnectedness of parts of ken back to Haeckel’s “law of recapitu- tions of patterns in early devel- different organ systems involved lation.” The next several decades will opmental stages) in critical functions) see the elaboration of more explicit 2. Genetic constraints (e.g., rates of descriptions of these hierarchical de- mutation and recombination of velopmental patterns. However, it is al- individual alleles) *Constraint is perhaps not the best term, ready becoming clear that such devel- for to constrain is not to restrain evolu- opmental stages (e.g., the zootypic 3. Direct developmental constraints tion. Constraints set limits to evolution, stage and the phylotypic stage) canal- (e.g., obligatory tissue interac- especially morphological evolution, but tions) groups with constrained characters are ize ontogenetic events to produce the among the most adaptively successful adult bauplan. This canalization comes 4. Cellular constraints (e.g., limits and speciose animal taxa.