Balfour, Garstang and de Beer: The First Century of Evolutionary Embryology

Evolution has been integrated with embryology during two greatperiods: the latter half of the 19th C as evolutionary morphology/embryology,and the latter third of the 20th C as evolutionary developmentalbiology. 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 foundationsof evolutionary embryology in the UK from 1870 (when "everyaspiring zoologist was an embryologist, and the one topic ofprofessional 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 ("homologyof phenotypes does not imply similarity in genotypes," de Beer,1971, p. 15). Evolutionary embryology was driven by a comparativeembryological approach that sought homology of adult structuresin germ layers and ancestry in embryos, and sought to differentiatelarval adaptations from retained ancestral characters. An initialemphasis on a phylogenetic mechanism (recapitulation) slowlygave way to more mechanistic approaches that included heterochronyand the integration of embryology with physiological genetics.Germ layers, homology, larval evolution, larval origins of thevertebrates, paedomorphosis and heterochrony underpinned theorigins of evolutionary embryology, and so I discuss each ofthese topics.     

Mechanistic Approaches to Community Ecology: A New Reductionism

Mechanistic approaches to community ecology are those whichemploy individual— ecological concepts—those ofbehavioral ecology, physiological ecology, and ecomorphology—as theoretical bases for understanding community patterns. Suchapproaches, which began explicitly about a decade ago, are justnow coming into prominence. They stand in contrast to more traditionalapproaches, such as MacArthur and Levins (1967),which interpretcommunity ecology almost strictly in terms of "megaparameters.". Mechanistic approaches can be divided into those which use populationdynamics as a major component of the theory and those whichdo not; examples of the two are about equally common. The firstapproach sacrifices a highly detailed representation of individual—ecological processes; the second sacrifices an explicit representationof the abundance and persistence of populations. Three subdisciplines of ecology—individual, populationand community ecology—form a "perfect" hierarchy in Beckner's(1974) sense. Two other subdisciplines—ecosystem ecologyand evolutionary ecology—lie somewhat laterally to thishierarchy. The modelling of community phenomena using sets ofpopulation-dynamical equations is argued as an attempt at explanationvia the reduction of community to population ecology. Much ofthe debate involving Florida State ecologists is over whetheror not such a relationship is additive (or conjunctive), a verystrong form of reduction. I argue that reduction of communityto individual ecology is plausible via a reduction of populationecology to individual ecology. Approaches that derive the population-dynamicalequations used in population and community ecology from individual-ecologicalconsiderations, and which provide a decomposition of megaparametersinto behavioral and physiological parameters, are cited as illustratinghow the reduction might be done. I argue that "sufficient parameters"generally will not enhance theoretical understanding in communityecology. A major advantage of the mechanistic approach is that variationin population and community patterns can be understood as variationin individual-ecological conditions. In addition to enrichingthe theory, this allows the best functional form to be chosenfor modeling higher-level phenomena, where "best" is definedas biologically most appropriate rather than mathematicallymost convenient. Disadvantages of the mechanistic approach arethat it may portend an overly complex, massive and special theory,and that it naturally tends to avoid many-species phenomenasuch as indirect effects. The paper ends with a scenario fora mechanistic-ecological utopia.     

Diachronic Biology Meets Evo-Devo: C. H. Waddington's Approach to Evolutionary Developmental Biology

Conrad Hal Waddington (1905–1975) did not respect thetraditional boundaries established between genetics, embryology,and evolutionary biology. Rather, he viewed them together asa "diachronic biology." In this diachronic biology, evolutionarychange was caused by heritable alterations in development. Stabilizingselection within the embryo was followed by normative selectionon the adult. To explain evolution, Waddington had to inventmany concepts and terms, some of which have retained their usageand some of which have not. In this paper I seek to explicateWaddington's ideas and evaluate their usefulness for contemporaryevolutionary developmental biology.     

Test of Von Baer's law of the conservation of early development

One of the oldest and most pervasive ideas in comparative embryology is the perceived evolutionary conservation of early ontogeny relative to late ontogeny. Karl Von Baer first noted the similarity of early ontogeny across taxa, and Ernst Haeckel and Charles Darwin gave evolutionary interpretation to this phenomenon. In spite of a resurgence of interest in comparative embryology and the development of mechanistic explanations for Von Baer's law, the pattern itself has been largely untested. Here, I use statistical phylogenetic approaches to show that Von Baer's law is an unnecessarily complex explanation of the patterns of ontogenetic timing in several clades of vertebrates. Von Baer's law suggests a positive correlation between ontogenetic time and amount of evolutionary change. I compare ranked position in ontogeny to frequency of evolutionary change in rank for developmental events and find that these measures are not correlated, thus failing to support Von Baer's model. An alternative model that postulates that small changes in ontogenetic rank are evolutionarily easier than large changes is tentatively supported.     

Model Systems versus Outgroups Alternative Approaches to the Study of Head Development and Evolution

There is widespread recognition of a recent coming togetherof developmental and evolutionary biology in the study of problemsof mutual interest. Contemporary studies into the developmentand evolution of the head largely comprise two parallel approaches,or research strategies the model systems approach and the comparativeapproach. The two strategies share the same general goal—greaterunderstanding of cranial development and evolution—buttypically emphasize different problems, ask different questions,and employ different methods, reflecting the contrasting backgroundsand biases of each group of investigators, there has been relativelylittle true synthesis. Each strategy is making important andvalid contributions, but both have limitations. Resolution ofmany fundamental and long-standing problems in cranial developmentand evolution will require a combined approach that incorporatesthe technical and conceptual strengths of each discipline.     

Experimental Evolution and Its Role in Evolutionary Physiology

Four general approaches to the study of evolutionary physiology—phylogenetically-basedcomparisons, genetic analyses and manipulations, phenotypicplasticity and manipulation, and selection studies—areoutlined and discussed. We provide an example of the latter,the application of laboratory selection experiments to the studyof a general issue in environmental adaptation, differencesin adaptive patterns of generalists and specialists. A cloneof the bacterium Escherichia coli that had evolved in a constantenvironment of 37°C was replicated into 6 populations andallowed to reproduce for 2,000 generations in a variable thermalenvironment alternating between 32 and 42°C. As predictedby theory, fitness and efficiency of resource use increasedin this new environment, as did stress resistance. Contraryto predictions, however, fitness and efficiency in the constantancestral environment of 37°C did not decrease, nor didthermal niche breadth or phenotypic plasticity increase. Selectionexperiments can thus provide a valuable approach to testinghypotheses and assumptions about the evolution of functionalcharacters.     

Evolutionary Morphology, Innovation, and the Synthesis of Evolutionary and Developmental Biology

One foundational question in contemporarybiology is how to `rejoin evolution anddevelopment. The emerging research program(evolutionary developmental biology or`evo-devo) requires a meshing of disciplines,concepts, and explanations that have beendeveloped largely in independence over the pastcentury. In the attempt to comprehend thepresent separation between evolution anddevelopment much attention has been paid to thesplit between genetics and embryology in theearly part of the 20th century with itscodification in the exclusion of embryologyfrom the Modern Synthesis. This encourages acharacterization of evolutionary developmentalbiology as the marriage of evolutionary theoryand embryology via developmental genetics. Butthere remains a largely untold story about thesignificance of morphology and comparativeanatomy (also minimized in the ModernSynthesis). Functional and evolutionarymorphology are critical for understanding thedevelopment of a concept central toevolutionary developmental biology,evolutionary innovation. Highlighting thediscipline of morphology and the concepts ofinnovation and novelty provides an alternativeway of conceptualizing the `evo and the `devoto be synthesized.     

Embryos in evolution: evo-devo at the Naples Zoological Station in 1874

Eighteen seventy-four was a high point in evolutionary embryology. Thanks to Charles Darwin, the theory of evolution by natural selection provided a revolutionary new way of viewing the relationships and origins of organisms on Earth. Thanks to Ernst Haeckel, embryos were the way to study evolution (Haeckel in Generelle morphologie der organismen, vols 1, 2. Verlag Georg Reimer, Berlin, 1866)—it really was embryos in evolution—and recapitulation was in the air. Thanks to Anton Dohrn, a new research facility was on the ground, designed, located and structured to facilitate the study of embryos in evolution. Anton Dohrn devised, designed, financed, supervised the construction and then administered the Naples Zoological Station specifically so that researchers from all nations would have a facility where Darwin’s theory of evolution by natural selection could be tested. The zoologists who took advantage of the brand new facility within weeks of its opening late in 1873 established lines of research into evolutionary embryology, the field we now know as evolutionary developmental biology (evo-devo), the study of embryos in evolution. I examine the approach taken by Ambrosius Hubrecht, the first Dutch embryologist to undertake research at the station, and then evaluate the research of three British zoologists—E. Ray Lankester, Albert Dew-Smith, and Francis Maitland (Frank) Balfour. All four sought insights into origins, especially vertebrate origins that rested on comparative embryology, homology, germ layers, and a Darwinian approach to origins.

Evolutionary developmental studies of cyclostomes and the origin of the vertebrate neck

Because they lack some gnathostome-specific traits, cyclostomes have often been regarded as representing an intermediate state linking non-vertebrate chordates and gnathostomes. To understand the evolutionary origins of the jaw and paired fins, lamprey embryos and larvae have been used as comparative models. The lack of the jaw–neck region is a conspicuous feature specific to cyclostomes; however, the absence of these features has been largely neglected both in evolutionary developmental studies and in the field of classical comparative embryology. This review seeks to develop a possible evolutionary scenario of the vertebrate neck muscles by taking the cucullaris (trapezius) muscle as the focus. By combining the comparative embryology of lampreys and gnathostomes, and considering the molecular-level developmental mechanism of skeletal muscle differentiation, this review argues that the establishment of the vertebrate neck deserves to be called an evolutionary novelty based on the remodeling of mesenchymal components between the cranium and the shoulder girdle, which involves both mesodermal and neural crest cell lineages.     

A Particular Synthesis: Aleksandr Promptov and Speciation in Birds

During the 1930s, Aleksandr Promptov—a student of the founder of Russian population genetics Sergei Chetverikov—developed an elaborate concept of speciation in birds. He conducted field investigations aimed at giving a naturalistic content to the theoretical formulations and laboratory models of evolutionary processes advanced within the framework of population genetics, placing particular emphasis on the evolutionary role of bird behavior. Yet, although highly synthetic in combining biogeographical, taxonomic, genetic, ecological, and behavioral studies, Promptov’s speciation concept was ignored by the architects of the 1930s and 1940s evolutionary synthesis, including Theodosius Dobzhnasky, Ernst Mayr, and Julian Huxley. In this article, I argue that the story of Promptov’s concept and its reception by other evolutionists challenges the traditional presentation of the synthesis as a singular, international process of the unification of biology, which led to the creation of a universal synthetic theory of evolution. It suggests that during the same time period, within largely the same theoretical framework, there were multiple, intrinsically local, attempts at creating synthetic evolutionary concepts. These concepts were often quite particular—in their taxonomic applicability, in their explanations of various evolutionary factors, and in the range of disciplines unified in the synthesis. Apparently, these concepts ran contrary to the universal aspirations of the synthesis architects, and as a result, they were disregarded, first by the architects and later by historians of the evolutionary synthesis.     

Evolutionary medicine at twenty: rethinking adaptationism and disease

Two decades ago, the eminent evolutionary biologist George C. Williams and his physician coauthor, Randolph Nesse, formulated the evolutionary medicine research program. Williams and Nesse explicitly made adaptationism a core component of the new program, which has served to undermine the program ever since, distorting its practitioners’ perceptions of evidentiary burdens and in extreme cases has served to warp practitioner’s understandings of the relationship between evolutionary benefits/detriments and medical ones. I show that the Williams and Nesse program more particularly embraces the panselectionist variety of adaptationism (the empirical assumption that non-adaptive evolutionary processes are causally unimportant compared to natural selection), and argue that this has harmed the field. Panselectionism serves to conceal the enormous evidentiary hurdles that evolutionary medicine hypotheses face, making them appear stronger than they are. I use two examples of evolutionary medicine texts, on neonatal jaundice and on asthma, to show that some evolutionary medicine practitioners have allowed their fervent panselectionism to directly shape their recommendations for clinical practice. I argue that this escalation of panselectionism’s influence is inappropriate under Williams’ and Nesse original stated standards, despite being inspired by their program. I also show that the examples’ conflation of clinical and evolutionary considerations is inappropriate even under Christopher Boorse’s controversial evolution-rooted concepts of disease and health.     

Systems for in vivo hypermutation: a quest for scale and depth in directed evolution

Traditional approaches to the directed evolution of genes of interest (GOIs) place constraints on the scale of experimentation and depth of evolutionary search reasonably achieved. Engineered genetic systems that dramatically elevate the mutation of target GOIs in vivo relieve these constraints by enabling continuous evolution, affording new strategies in the exploration of sequence space and fitness landscapes for GOIs. We describe various in vivo hypermutation systems for continuous evolution, discuss how different architectures for in vivo hypermutation facilitate evolutionary search scale and depth in their application to problems in protein evolution and engineering, and outline future opportunities for the field.     

Bio-monitoring of ozone by young students

The inquiry-based approach is an important component of secondary school biology curricula. However, we found that common Australian texts included little coverage of controlled experimentation in ecological practical work. The logistical and ethical difficulties in designing suitable ecological practicals may be a factor in these observations, as well as a perception that investigations of the complex interrelationships in ecology require scientific approaches other than experimentation. We argue that because controlled experiments are used extensively by professional ecologists to solve both theoretical and applied problems, experimentation should be a key component of secondary school ecology curricula. We suggest five teaching principles to guide secondary school biology teachers in providing a more realistic view of the possibilities and limitations of ecological experimentation. We also review ways in which computer simulations and microcosm experiments can be used to overcome logistical and ethical problems and allow students to design and implement ecological experiments. Whether based in the classroom or the field, the use of experimental approaches in secondary school ecology curricula illustrates ecological concepts, reinforces principles of experimental design and highlights the value of the inquiry-based approach in biological education.     

Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of evo-devo

Alexander Kowalevsky was one of the most significant 19th century biologists working at the intersection of evolution and embryology. The reinstatement of the Alexander Kowalevsky Medal by the St. Petersburg Society of Naturalists for outstanding contributions to understanding evolutionary relationships in the animal kingdom, evolutionary developmental biology, and comparative zoology is timely now that Evo-devo has emerged as a major research discipline in contemporary biology. Consideration of the intellectual lineage of comparative evolutionary embryology explicitly forces a reconsideration of some current conceptions of the modern emergence of Evo-devo, which has tended to exist in the shadow of experimental embryology throughout the 20th century, especially with respect to the recent success of developmental biology and developmental genetics. In particular we advocate a sharper distinction between the heritage of problems and the heritage of tools for contemporary Evo-devo. We provide brief overviews of the work of N. J. Berrill and D. T. Anderson to illustrate comparative evolutionary embryology in the 20th century, which provides an appropriate contextualization for a conceptual review of our research on the sea urchin genus Heliocidaris over the past two decades. We conclude that keeping research questions rather than experimental capabilities at the forefront of Evo-devo may be an antidote to any repeat of the stagnation experienced by the first group of evolutionary developmental biologists over one hundred years ago and acknowledges Kowalevsky's legacy in evolutionary embryology.     

Microbial Symbiosis: Patterns of Diversity in the Marine Environment

SYNOPSIS. Symbiotic associations expand both the diversity ofpotential ecological niches and metabolic capabilities of thehost—symbiont combinations. Symbioses can also be consideredto have evolutionary potential in that the partnership can resultin a "new organism." Associations between chemoautotrophic bacteriaand marine invertebrates, discovered only 10 years ago, arenow found widely in nature, in habitats ranging from deep-seahydrothermal vents to coastal sediments. Here I review chemoautotroph—invertebrateassociations and discuss the benefits inferred for both partnerswith regard to the diversity of these symbioses in nature.     

Coordinating the traditional and modern approaches in the systematics of insects

The problem of coordinating the traditional and modern approaches to systematics is ever-lasting due to the continuous development and enrichment of our knowledge of biodiversity, means of analysis, and concepts. Comparative morphology was and still is the cornerstone of studies of insect taxonomy. It gives the most extensive and diverse information on the organisms studied, particularly when it is supported by the data on embryology and functional morphology as well as by analysis of adaptive significance of morphological characters. The limitations of this approach are often related to the presence of homoplasies, reversions, etc. Comparative paleontology is the only approach providing direct evidence of the historical succession of taxa and their characters. However, this approach is fully applicable only to some groups due to the specific features of their morphology and taphonomy. All the modern approaches (molecular, cytogenetic, etc.) are very informative but also have their own limitations; they should not be contrasted with the traditional approaches and certainly should not replace them. The traditional approaches do not become obsolete; it is only their comparative importance in the set of taxonomic tools that may be reevaluated. No single approach can be considered universal for an unambiguous reconstruction of phylogeny and substantiation of the natural system of taxa. Each approach has its own advantages and limitations, and only combined use of different approaches allows a broader range of the problems to be solved. Different approaches may prevail in the studies of different groups of insects and at different levels of taxonomic hierarchy. The intuition of the taxonomist, which is so often criticized by the followers of “objective” systematics, is based on taxonomic experience and scope of knowledge of a particular taxon. It does not imply a subjective bias, but allows the taxonomist to choose the instruments adequate to a particular case.     

How and When Selection Experiments Might Actually be Useful

Laboratory natural selection and artificial selection are vitaltools for addressing specific questions about evolutionary patternsof variation. Laboratory natural selection can illuminate whethera putative selective agent is capable of generating long-term,sustained changes in individual traits and suites of traits.Artificial selection is the essential tool for understandingthe general evolvability of traits and the extent to which geneticcorrelations constrain evolution. We review the contexts inwhich each type of experiment seems capable of offering keyinsights into important evolutionary issues. We also discusstheoretical and methodological considerations that play criticalroles in designing selection experiments that are relevant toevolutionary patterns of trait variation. In particular, wefocus on the critical role of selection intensity and the consequencesof experiments with different intensities. While selection experimentsare not practical in many cases, sophisticated selection experiments—designedwith careful consideration of the theory of selection—shouldbe taken beyond model organisms and used in well-chosen naturalsystems to understand natural patterns of variation.     

Tribute to Tinbergen: The Place of Animal Behavior in Biology

Tinbergen is famous for emphasizing behavioral fieldwork and experimentation under natural circumstances, for founding the field of ethology, for getting a Nobel Prize, and for mentoring Richard Dawkins. He is known for dividing behavior studies into physiology, development, natural selection, and evolutionary history. In the decades since Tinbergen was active, some of the best research in animal behavior fuses Tinbergen's questions, connecting genes to behavioral phenotypes, for example. Behavior is the most synthetic of the life sciences, because observing the actions of an organism can tell us what all those physical and physiological traits are for. Insights from behavior tell us how traits in one individual impact those in another in ways that challenge our definition of an organism. Behavioral conflict and cooperation among animals has led to theory that explains within‐organism conflict and cooperation and human malfunctions of many kinds. Darwin certainly began the evolutionary study of behavior, but Tinbergen brought it forward to the heart of biology. The challenge for the future is to apply concepts from animal behavior across biology with tools that would have amazed Tinbergen.