The excluded philosophy of evo-devo? Revisiting C.H. Waddington's failed attempt to embed Alfred North Whitehead's "organicism" in evolutionary biology

Though a prominent British developmental biologist in his day, a close friend of Theodosius Dobzhansky, and a frequent correspondent with Ernst Mayr, C.H. Waddington did not enter the ranks of "architect" of the Modern Synthesis. By the end of his career, in fact, he recognized that other biologists reacted to his work "as though they feel obscurely uneasy"; and that the best that some philosophers of biology could say of his work was that he was not "wholly orthodox" (Waddington 1975c, 11). In this essay, I take Waddington's self-assessments at face value and explore three potential reasons why his work did not have more of a direct impact: Waddington's explicit support for the philosophy of Alfred North Whitehead; a lack of institutional support; and Waddington's occasional marginalization from the core network of American neo-Darwinians. Though excluded from the Modern Synthesis in the mid-20th century, it now appears that Waddington's work does undergird the emerging evo-devo synthesis. Whether this indicates concomitant, if implicit, support for Whiteheadian philosophy is an interesting question not explored here.     

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.     

Waddington's widget: Hsp90 and the inheritance of acquired characters

Conrad Waddington published an influential model for evolution in his 1942 paper, Canalization of Development and Inheritance of Acquired Characters. In this classic, albeit controversial, paper, he proposed that an unknown mechanism exists that conceals phenotypic variation until the organism is stressed. Recent studies have proposed that the highly conserved chaperone Hsp90 could function as a "capacitor," or an "adaptively inducible canalizer," that masks silent phenotypic variation of either genetic or epigenetic origin. This review will discuss evidence for, and arguments against, the role of Hsp90 as a capacitor for morphological evolution, and as a key component of what we call "Waddington's widget."     

The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity

Two different, but related, evolutionary theories pertaining to phenotypic plasticity were proposed by James Mark Baldwin and Conrad Hal Waddington. Unfortunately, these theories are often confused with one another. Baldwin's notion of organic selection posits that plasticity influences whether an individual will survive in a new environment, thus dictating the course of future evolution. Heritable variations can then be selected upon to direct phenotypic evolution (i.e., "orthoplasy"). The combination of these two processes (organic selection and orthoplasy) is now commonly referred to as the "Baldwin effect." Alternately, Waddington's genetic assimilation is a process whereby an environmentally induced phenotype, or "acquired character," becomes canalized through selection acting upon the developmental system. Genetic accommodation is a modern term used to describe the process of heritable changes that occur in response to a novel induction. Genetic accommodation is a key component of the Baldwin effect, and genetic assimilation is a type of genetic accommodation. I here define both the Baldwin effect and genetic assimilation in terms of genetic accommodation, describe cases in which either should occur in nature, and propose that each could play a role in evolutionary diversification.     

Michael Akam and the rise of evolutionary developmental biology

Michael Akam has been awarded the 2007 Kowalevsky medal for his many research accomplishments in the area of evolutionary developmental biology. We highlight three tributaries of Michael’s contribution to evolutionary developmental biology. First, he has made major contributions to our understanding of development of the fruit fly, Drosophila melanogaster. Second, he has maintained a consistent focus on several key problems in evolutionary developmental biology, including the evolving role of Hox genes in arthropods and, more recently, the evolution of segmentation mechanisms. Third, Michael has written a series of influential reviews that have integrated progress in developmental biology into an evolutionary perspective. Michael has also made a large impact on the field through his effective mentorship style, his selfless promotion of younger colleagues, and his leadership of the University Museum of Zoology at Cambridge and the European community of evolutionary developmental biologist.     

Walter Garstang: a retrospective

Although, Walter Garstang died over 60 years ago, his work is still cited—sometimes praised, but sometimes belittled. On the negative side, he often appropriated ideas of others without attribution, ignored earlier studies conflicting with his theories, and clung to notions like inheritance of acquired characters, progressive evolution, and saltation after many of his contemporaries were advancing toward the modern synthesis. Moreover, his evolutionary scenarios—especially his derivation of vertebrates from a sessile ascidian—have not been well supported by recent work in developmental genetics and molecular phylogenetics. On the positive side, Garstang firmly established several points of view that remain useful in the age of evolutionary development (evo-devo). He popularized the valid idea that adaptive changes in larvae combined with shifts in developmental timing (heterochrony) could radically change adult morphology and provide an escape from overspecialization. Moreover, his re-statement of the biogenetic law is now widely accepted: namely, that recapitulation results when characters at one stage of development are required for the correct formation of other characters at subsequent stages (his stepping stone model). In other words, ontogeny creates phylogeny because some developmental features are constraints, favoring particular evolutionary outcomes while excluding others. This viewpoint is a useful basis for advancing concepts of homology and for comparing the phylogeny of ontogenies across a series of animals to ascertain the timing and the nature of the underlying ontogenetic changes.     

Epigenetic landscaping: Waddington's use of cell fate bifurcation diagrams

From the 1930s through the 1970s, C. H. Waddington attempted to reunite genetics, embryology, and evolution. One of the means to effect this synthesis was his model of the epigenetic landscape. This image originally recast genetic data in terms of embryological diagrams and was used to show the identity of genes and inducers and to suggest the similarities between embryological and genetic approaches to development. Later, the image became more complex and integrated gene activity and mutations. These revised epigenetic landscapes presented an image of how mutations could alter developmental pathways to yield larger phenotypic changes. These diagrams became less important as the operon became used to model differential gene regulation.     

Epistemic and community transition in American evolutionary studies: the ‘Committee on Common Problems of Genetics,Paleontology, and Systematics’ (1942–1949)

The Committee on Common Problems of Genetics, Paleontology, and Systematics (United States National Research Council) marks part of a critical transition in American evolutionary studies. Launched in 1942 to facilitate cross-training between genetics and paleontology, the Committee was also designed to amplify paleontologist voices in modern studies of evolutionary processes. During coincidental absences of founders George Gaylord Simpson and Theodosius Dobzhansky, an opportunistic Ernst Mayr moved into the project’s leadership. Mayr used the opportunity for programmatic reforms he had been pursuing elsewhere for more than a decade. These are evident in the Bulletins he distributed under Committee auspices. In his brief tenure as Committee leader, Mayr gained his first substantial foothold within the coalescing community infrastructure of evolutionary studies. Carrying this momentum forward led Mayr directly into the project to launch the journal Evolution. The sociology of interdisciplinary activity provides useful tools for understanding the Committee’s value in the broad sweep of change in evolutionary studies during the synthesis period.     

Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history

Understanding how traits are integrated at the organismal level remains a fundamental problem at the interface of developmental and evolutionary biology. Hormones, regulatory signaling molecules that coordinate multiple developmental and physiological processes, are major determinants underlying phenotypic integration. The probably best example for this is the lipid-like juvenile hormone (JH) in insects. Here we review the manifold effects of JH, the most versatile animal hormone, with an emphasis on the fruit fly Drosophila melanogaster, an organism amenable to both genetics and endocrinology. JH affects a remarkable number of processes and traits in Drosophila development and life history, including metamorphosis, behavior, reproduction, diapause, stress resistance and aging. While many molecular details underlying JH signaling remain unknown, we argue that studying "hormonal pleiotropy" offers intriguing insights into phenotypic integration and the mechanisms underlying life history evolution. In particular, we illustrate the role of JH as a key mediator of life history trade-offs.     

Nikolaĭ Vladimirovich Timofeev-Resovskiĭ (1900-1981). (Essay on his life and works)

The article contains a brief review of the basic works (1925-1981) written by Nikolay V. Timofeeff-Ressovsky--one of the famous geneticist of the elapsing century, the founder of radiobiology and radiation genetics, biocenology and radioecology, a prominent evolutionary biologist. In genetics, his name is associated with the development of fundamental problems of population genetics, phenogenetics, gene interaction and investigations of the role of environmental and genetic factors in expression of different characters. Timofeeff-Ressovsky classical works on mutagenesis process and especially, radiation mutagenesis, promoted penetration of methods and approaches applied in molecular physics and chemistry, into genetic analysis, and accelerated forming of the modern molecular genetics. A special place in the development of population genetics is occupied by the hypothesis of microevolutionary process developed by Nikolay V. Timofeeff-Ressovsky along with other famous biologists in the end of the 30-ies. This hypothesis connected Darwin's evolutionary theory with rapidly developing concepts of genetics. In the last years of his life, Timofeeff-Ressovsky was especially interested in a global problem which was called by him "The Biosphere and Humanity". Here was especially strikingly shown the broadness of his approach to the analysis of the biosphere phenomena in the best traditions of the Russian natural science. In the course of time, the wealth of Nikolay V. Timofeeff-Ressovsky's scientific heritage not only remains valuable, but also takes on more profundity and value.     

Jonathan Hodgkin

Jonathan Hodgkin graduated from Oxford in 1971 and then did a PhD with Sydney Brenner at MRC LMB in Cambridge, studying behavioural genetics in the nematode Caenorhabditis elegans. Later, after a couple of years working with myxobacteria as a postdoc in Dale Kaiser's lab at Stanford, he returned to LMB as a staff member, where he remained for most of the subsequent two decades. In the year 2000, he moved to Oxford as Professor of Genetics in the Department of Biochemistry, switching his major research interests from developmental genetics and sex determination to the study of host-pathogen interactions in the worm. For the past ten years, he has acted as curator of the C. elegans genetic map and gene nomenclature, and he is currently President of the Genetics Society of Great Britain.     

Garland Allen,Thomas Hunt Morgan,and Development

Garland E. Allen’s 1978 biography of the Nobel Prize winning biologist Thomas Hunt Morgan provides an excellent study of the man and his science. Allen presents Morgan as an opportunistic scientist who follows where his observations take him, leading him to his foundational work in Drosophila genetics. The book was rightfully hailed as an important achievement and it introduced generations of readers to Morgan. Yet, in hindsight, Allen’s book largely misses an equally important part of Morgan’s work – his study of development and regeneration. It is worth returning to this part of Morgan, exploring what Morgan contributed and also why he has been seen by contemporaries and historians such as Allen as having set aside some of the most important developmental problems. A closer look shows how Morgan’s view of cells and development that was different from that of his most noted contemporaries led to interpretation of his important contributions in favor of genetics. This essay is part of a special issue, revisiting Garland Allen's views on the history of life sciences in the twentieth century.     

From Hopeful Monsters to Homeotic Effects: Richard Goldschmidt's Integration of Development, Evolution, and Genetics

Richard Goldschmidt's research on homeotic mutants from 1940until his death in 1958 represents one of the first seriousefforts to integrate genetics, development, and evolution. Usingtwo different models, Goldschmidt tried to show how differentviews of genetic structure and gene action could provide a mechanismfor rapid speciation. Developmental systems were emphasizedin one model and a hierarchy of genetic structures in the other.While Goldschmidt tried to find a balance between developmentand genetics, critics, such as Sewall Wright, urged him andeventually helped him incorporate population dynamics into hismodels as well. As such, the history of Goldschmidt's researchon homeotic mutants highlights the continuing challenge of producinga balanced and integrated developmental evolutionary genetics.     

Evolution of ontogeny and nature of heterochronies

Every aspect of biological orderliness is a result of evolution, which expresses the systemic reorganization of organismal body plan, along with the way of its ontogenetic formation. Phyletic changes in the developmental rates (heterochronies) experienced by the organism or its structures exemplify just a kind of such consequences. The current belief that heterochronies are the causes of evolutionary events is based on the assumption that evolution of ontogeny proceeds in the same way as the ontogeny itself, i.e., from a germ cell to adult state. This premise (termed here “the central dogma”) is the cornerstone of traditional ideas of the evolutionary mechanism, regardless of whether it is perceived in terms of gene mutations or “embryonic modes.” In fact, the directions of two transformations compared are opposite each other. An evolutionary change in the body plan results from reorganization of the developmental system, which comes in response to disturbance of stability of the system’s terminal (adult) state. Realized by selection, this change starts immediately from the terminal state and then spreads in generations towards early ontogenetic stages. Heterochronies show just the same dynamics of events irrespective of whether they reflect the acceleration or delay of development. Empirically, such course of evolutionary changes was grounded most evidently by Severtsov in the early version of his concept of the phylembryogenesis. The theoretical basis of the same regularity is provided by the Schmalhausen–Waddington’s theory.     

From the "Modern Synthesis" to cybernetics: Ivan Ivanovich Schmalhausen (1884-1963) and his research program for a synthesis of evolutionary and developmental biology

Ivan I. Schmalhausen was one of the central figures in the Russian development of the "Modern Synthesis" in evolutionary biology. He is widely cited internationally even today. Schmalhausen developed the main principles of his theory facing the danger of death in the totalitarian Soviet Union. His great services to evolutionary and theoretical biology are indisputable. However, the received view of Schmalhausen's contributions to evolutionary biology makes an unbiased reading of his texts difficult. Here we show that taking all of his works into consideration (including those only available in Russian) paints a much more dynamic and exciting picture of what he tried to achieve. Schmalhausen pioneered the integration of a developmental perspective into evolutionary thinking. A main tool for achieving this was his approach to living objects as complex multi-level self-regulating systems. Schmalhausen put enormous effort into bringing this idea into fruition during the final stages of his career by combining evolutionary theory with cybernetics. His results and ideas remain thought-provoking, and his texts are of more than just historical interest.     

In search of evolutionary developmental mechanisms: the 30-year gap between 1944 and 1974

The approach I have elected in this retrospective of how I became a student of evo-devo is both biographical and historical, a case study along the lines of Waddington's The Evolution of an Evolutionist ('75), although in my case it is the Evolution of an Evo-devoist. What were the major events that brought me to developmental biology and from there to evo-devo? They were, of course, specific to my generation, to the state of knowledge at the time, and to my own particular circumstances. Although exposed to evolution and embryology as an undergraduate in the 1960s, my PhD and post-PhD research programme lay within developmental biology until the early 1970s. An important formative influence on my studies as an undergraduate was the work of Conrad Hal Waddington (1905-1975), whose writings made me aware of genetic assimilation and gave me an epigenetic approach to my developmental studies. The switch to evo-devo (and my discovery of the existence of the neural crest), I owe to an ASZ (now SICB) symposium held in 1973.     

Alfred Kühn (1885-1968) and developmental evolution

Alfred Kühn (1885-1968) was known as one of the most comprehensive zoologists of his time. His research program in developmental physiological genetics was one of the first successful attempts to integrate the experimental study of development and heredity. It led him to discover the first known reaction chain from gene to phenotype. Kühn also foresaw many elements of modern evolutionary developmental biology and as a student of Weismann and mentor to many developmental geneticists of the late 20th century directly connects Weismann with molecular developmental genetics.     

Between Biochemists and Embryologists – The Biochemical Study of Embryonic Induction in the 1930s

The discovery by Hans Spemann of the “organizer” tissue and its ability to induce the formation of the amphibian embryo’s neural tube inspired leading embryologists to attempt to elucidate embryonic inductions’ underlying mechanism. Joseph Needham, who during the 1930s conducted research in biochemical embryology, proposed that embryonic induction is mediated by a specific chemical entity embedded in the inducing tissue, surmising that chemical to be a hormone of sterol-like structure. Along with embryologist Conrad H. Waddington, they conducted research aimed at the isolation and functional characterization of the underlying agent. As historians clearly pointed out, embryologists came to question Needham’s biochemical approach; he failed to locate the hormone he sought and eventually abandoned his quest. Yet, this study finds that the difficulties he ran into resulted primarily from the limited conditions for conducting his experiments at his institute. In addition, Needham’s research reflected the interests of leading biochemists in hormone and cancer research, because it offered novel theoretical models and experimental methods for engaging with the function of the hormones and carcinogens they isolated. Needham and Waddington were deterred neither by the mounting challenges nor by the limited experimental infrastructure. Like their colleagues in hormone and cancer research, they anticipated difficulties in attempting to establish causal links between complex biological phenomena and simple chemical triggering.     

Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plans and evolvability

This paper reviews the scientific career of Rupert Riedl and his contributions to evolutionary biology. Rupert Riedl, a native of Vienna, Austria, began his career as a marine biologist who made important contributions to the systematics and anatomy of major invertebrate groups, as well as to marine ecology. When he assumed a professorship at the University of North Carolina in 1968, the predominant thinking in evolutionary biology focused on population genetics, to the virtual exclusion of most of the rest of biology. In this atmosphere Riedl developed his "systems theory" of evolution, which emphasizes the role of functional and developmental integration in limiting and enabling adaptive evolution by natural selection. The main objective of this theory is to account for the observed patterns of morphological evolution, such as the conservation of body plans. In contrast to other "alternative" theories of evolution, Riedl never denied the importance of natural selection as the driving force of evolution, but thought it necessary to contextualize natural selection with the organismal boundary conditions of adaptation. In Riedl's view development is the most important factor besides natural selection in shaping the pattern and processes of morphological evolution.     

Conrad Hal Waddington: the last Renaissance biologist?

Conrad Hal Waddington was a leading embryologist and geneticist from the 1930s to the 1950s. He is remembered mainly for his concepts of the 'epigenetic landscape' and 'genetic assimilation'. This article reviews his life and work, and enquires to what extent his ideas are relevant tools for understanding the biological problems of today.