This symposium undertakes to examine some historical background relevant to the renaissance in biological studies linking evolution and development, to review the current status of research in this rapidly changing area (especially the problem of forging links between disciplines that have gone in divergent directions), to address the benefits and difficulties that arise from molecular studies of the relationship between evolution and development, and to help set the research agenda in evolutionary developmental biology in the next few years. Rather than introducing the individual contributions that follow, this paper aims to set some historical background for the topics they cover. I argue that old questions about the relationship of development to evolution, raised by such figures as William Bateson and Richard Goldschmidt, remain relevant to contemporary work, though they require major reformulation in light of subsequent developments. Many older questions, long set aside as intractable, remain open. Recently developed techniques may enable us to answer some of them. Accordingly, I suggest, it is worth reviewing the work of several historical figures in setting current research agendas.

Evolution has been integrated with embryology during two great periods: the latter half of the 19th C as evolutionary morphology/embryology, and the latter third of the 20th C as evolutionary developmental biology. My mandate was to use the contributions of three embryologists/morphologists: Francis (Frank) Balfour (1851–1882), Walter Garstang (1868–1949) and Gavin de Beer (1899–1972) to discuss the foundations of evolutionary embryology in the UK from 1870 (when “every aspiring zoologist was an embryologist, and the one topic of professional conversation was evolution,” Bateson, 1922, p. 56), through the 1920s (“ontogeny does not recapitulate phylogeny, it creates it,” Garstang, 1922, p. 81) to the 1970s (“homology of phenotypes does not imply similarity in genotypes,” de Beer, 1971, p. 15). Evolutionary embryology was driven by a comparative embryological approach that sought homology of adult structures in germ layers and ancestry in embryos, and sought to differentiate larval adaptations from retained ancestral characters. An initial emphasis on a phylogenetic mechanism (recapitulation) slowly gave way to more mechanistic approaches that included heterochrony and the integration of embryology with physiological genetics. Germ layers, homology, larval evolution, larval origins of the vertebrates, paedomorphosis and heterochrony underpinned the origins of evolutionary embryology, and so I discuss each of these topics.

Conrad Hal Waddington (1905–1975) did not respect the traditional boundaries established between genetics, embryology, and evolutionary biology. Rather, he viewed them together as a “diachronic biology.” In this diachronic biology, evolutionary change was caused by heritable alterations in development. Stabilizing selection within the embryo was followed by normative selection on the adult. To explain evolution, Waddington had to invent many concepts and terms, some of which have retained their usage and some of which have not. In this paper I seek to explicate Waddington's ideas and evaluate their usefulness for contemporary evolutionary developmental biology.

Richard Goldschmidt's research on homeotic mutants from 1940 until his death in 1958 represents one of the first serious efforts to integrate genetics, development, and evolution. Using two different models, Goldschmidt tried to show how different views of genetic structure and gene action could provide a mechanism for rapid speciation. Developmental systems were emphasized in one model and a hierarchy of genetic structures in the other. While Goldschmidt tried to find a balance between development and genetics, critics, such as Sewall Wright, urged him and eventually helped him incorporate population dynamics into his models as well. As such, the history of Goldschmidt's research on homeotic mutants highlights the continuing challenge of producing a balanced and integrated developmental evolutionary genetics.

Synopsis. Allometry designates the changes in relative dimensions of parts of the body that are correlated with changes in overall size. Julian Huxley and Georges Teissier coined this term in 1936. In a joint paper, they agreed to use this term in order to avoid confusion in the field of relative growth. They also agreed on the conventional symbols to use in the algebraic formula: y = bx^α. Julian Huxley is often said to have discovered the “law of constant differential growth” in 1924, but a similar formula had been used earlier by several authors, in various contexts, and under various titles. Three decades before Huxley, Dubois and Lapicque used a power law and logarithmic coordinates for the description of the relation between brain size and body size in mammals, both from an intraspecific, and an interspecific, point of view. Later on, in the 1910s and early 1920s, Pézard and Champy's work on sexual characters provided decisive experimental evidence in favor of a law of relative growth at the level of individual development.

This paper examines: (1) early works on relative growth, and their relation to Huxley and Teissier's “discovery”; (2) Teissier and Huxley's joint paper of 1936, in particular their tacit disagreement on the signification of the coefficient “b”; and (3) the status of allometry in evolutionary theory after Huxley, especially in the context of paleobiology.

Much attention has been paid to the role of developmental information in estimating phylogenetic relationships and, more recently, to the use of phylogenies in understanding the evolution of development. At the moment, however, we lack a sufficiently general theory connecting phylogenetic patterns of character evolution to properties of developmental systems. Here we outline a simple model relating homoplasy to the rate of character change and the number of evolvable states, both of which may reflect developmental constraints. Given a particular rate of character change, the fewer the evolvable states the more homoplasy is expected, and vice versa. The repeated evolution of a limited number of forms of bilateral flower symmetry may reflect constraints imposed by overall flower orientation and underlying mechanisms of differentiation.

The concept of modularity is fundamental to research in both evolutionary and developmental biology, though workers in each field use the idea in different ways. Although readily and intuitively recognized, modularity is difficult to define precisely. Most definitions of modularity are operational and implicit, particularly in developmental biology. Examination of several proposed definitions points to some general characteristics of developmental modules, for example their internal integration, and suggests the importance of devising a definition applicable at different levels of the biological hierarchy. Modules, like homologs, must be defined with respect to a specified level of the hierarchy, and a general definition should support both analyses of the evolving causal relationships between levels, and studies of the interconnections between modules of the same type. The designation of a developmental structure, process, or function as a “module” is a testable hypothesis; this hypothesis is confirmed in the case of the dorsal marginal zone of the amphibian gastrula, which acts as a morphogenetic module. Discussions of developmental modularity can provide a meeting place for developmental and evolutionary biologists by helping us articulate key questions at the intersection of the two fields, and design experiments to begin answering them.

Homology is a central concept for Developmental Evolution. Here I argue that homology should be explained within the reference processes of development and evolution; development because it is the proximate cause of morphological characters and evolution because it deals with organic transformations and stability. This was already recognized by Hans Spemann in 1915. In a seminal essay “A history and critique of the homology concept” Spemann analyzed the history and present problems of the homology concept. Here I will continue Spemann's project and analyze some of the 20th century contributions to homology. I will end with a few reflections about the connections between developmental processes and homology and conclude that developmental processes are inherent in (i) the assessment of homology, (ii) the explanation of homology, (iii) the origin of evolutionary innovations (incipient homologues), and (iv) can be considered homologous themselves.

Among the primary contributions of phylogenetic systematics to the synthesis of developmental biology and evolution are phylogenetic hypotheses. Phylogenetic hypotheses are critical in interpreting the patterns of evolution of developmental genes and processes, as are morphological data. Using a robust phylogeny, the evolutionary history of individual morphological or developmental features can be traced and ancestral conditions inferred. Multiple characters (e.g., morphological and developmental) can be mapped together on the phylogeny, and patterns of character association can be quantified and tested for correlation.

Using the vertebrate forelimb as an example, I show that by mapping accurate morphological data (homologous skeletal elements of the vertebrate forelimb) onto a phylogeny, an alternative interpretation of Hox gene expression emerges. Teleost fishes and tetrapods may share no homologous skeletal elements in their forelimbs, and thus similarities and differences in Hox patterns during limb development must be reinterpreted. Specifically, the presence of the phase III Hox pattern in tetrapods may not be correlated with digits but rather may simply be the normal expression pattern of a metapterygium in fishes. This example illustrates the rigorous hypotheses that can be developed using morphological data and phylogenetic methods.

“Creating a general reference system and investigating the relations that extend from it to all other possible and necessary systems in biology is the task of systematics.” (Hennig, 1966, p.7)

Morphometric approaches facilitate the analysis of quantitative variation in form, typically becoming most useful for the study of organisms that have completed morphogenesis and are at differing stages of growth. Recent conceptual and technical refinements in the characterization and comparison of forms have joined methodological innovations in molecular biology, embryology, and phylogeny reconstruction to advance the study of the evolution of development. Among the phenomena that have recently been examined morphometrically are developmental integration and heterochrony, discoveries that in turn raise deeper questions about the connections among disciplines and among levels of description: the relationship between morphometric variables and characters, between phenomenology and process, and the interplay (and evolutionary relevance) of genes and phenotypes. Morphometrics can continue to play a vital role in evolutionary studies of development as its results generate questions both for its practitioners and for other sorts of biologists to explore.

Evolutionary developmental biology is inevitably a comparative subject. However, the taxonomic level at which comparisons can be made varies widely, and this greatly affects the kind of information that can be gained from the comparison. Broadly speaking, high-level comparisons (e.g., between phyla) are more informative about phylogenetic pattern and homology, while low-level comparisons (e.g., between congeneric species) are more informative about evolutionary mechanisms, including speciation. However, so far evolutionary developmental biology has had a relatively minor input into the traditional territory of population genetics, namely comparisons within species—both within and between geographic populations. Yet this area is crucial, as all evolutionary novelties ultimately arise from intraspecific variation. Here, I address this issue, focusing on the question of how early in development novelties arise. To shed light on this question, I discuss two examples of developmental polymorphism within species involving two of the main body axes: anteroposterior segmentation in centipedes and left–right asymmetry (chirality) in gastropods.

Developmental Evolution (DE) contributes to various research programs in biology, such as the assessment of homology and the determination of the genetic architecture underlying species differences. The most distinctive contribution offered by DE to evolutionary biology, however, is the elucidation of the role of developmental mechanisms in the origin of evolutionary innovations. To date, explanations of evolutionary innovations have remained beyond the reach of classical evolutionary genetics, because such explanations require detailed information on the function of genes and the emergent developmental dynamics of their interactions with other genetic factors. We argue that this area has the potential to become the core of DE's disciplinary identity. The main challenge in developing a research program for DE along these lines, however, is to provide a methodological framework that accounts for the fact that developmental mechanisms continue to evolve after a character has originated. Developmental mechanisms elucidated in a derived species may therefore not provide insights into the evolutionary origin of the character in question. To meet this challenge, we propose a set of questions that may guide us in our search for valid inferences on the role of developmental mechanisms in the explanation of evolutionary innovations.