Ehud Lamm

The Nurture of Nature: Hereditary Plasticity in Evolution

The dichotomy between Nature and Nurture, which has been dismantled within the framework of development, remains embodied in the notions of plasticity and evolvability. We argue that plasticity and evolvability, like development and heredity, are neither dichotomous nor distinct: the very same mechanisms may be involved in both, and the research perspective chosen depends to a large extent on the type of problem being explored and the kinds of questions being asked. Epigenetic inheritance leads to transgenerationally extended plasticity, and developmentally-induced heritable epigenetic variations provide additional foci for selection that can lead to evolutionary change. Moreover, hereditary innovations may result from developmentally induced large-scale genomic repatterning events, which are akin to Goldschmidtian “systemic mutations”. The epigenetic mechanisms involved in repatterning can be activated by both environmental and genomic stress, and lead to phylogenetic as well as ontogenetic changes. Hence, the effects and the mechanisms of plasticity directly contribute to evolvability.

Commentary: The epigenotype—a dynamic network view of development

During the late 1930s and the early 1940s, a particularly productive period in his scientific life, Conrad Hal Waddington (1905–75) started to construct a new synthesis between genetics, embryology and evolution. In the 4 years between 1939 and 1943, before he became involved in military activity during the Second World War, he published two substantial books and several seminal papers, all of which were explicitly geared towards constructing of an integrated view of biology. ‘The Epigenotype’, 1 published in 1942 in the semi-popular science journal Endeavour, is one of these papers. In it, Waddington presented and developed some of the ideas that he had already discussed in his books, and also defined, albeit informally, a new domain of research, epigenetics—the study of the causal mechanisms intervening between the genotype and the phenotype. Today, epigenetics is a very broad field of study, covering many aspects of biology, including morphogenesis, cell heredity, transgenerational epigenetic inheritance, and the evo-devo approach to evolution that Waddington investigated though his genetic assimilation experiments. In this commentary, we briefly discuss one particular aspect of Waddington’s epigenetic approach, the network-oriented view that he put forward in the 1942 Endeavour paper, 1 and the way in which this network view, Waddington’s epigenotype, is conceived today.

The genome as a developmental organ

This paper applies the conceptual toolkit of Evolutionary Developmental Biology (evo‐devo) to the evolution of the genome and the role of the genome in organism development. This challenges both the Modern Evolutionary Synthesis, the dominant view in evolutionary theory for much of the 20th century, and the typically unreflective analysis of heredity by evo‐devo. First, the history of the marginalization of applying system‐thinking to the genome is described. Next, the suggested framework is presented. Finally, its application to the evolution of genome modularity, the evolution of induced mutations, the junk DNA versus ENCODE debate, the role of drift in genome evolution, and the relationship between genome dynamics and symbiosis with microorganisms are briefly discussed.

Integrating Evolution and Development: From Theory to Practice

This volume joins a growing list of books, monographs, and proceedings from scientific meetings that attempt to consolidate the wide spectrum of approaches emphasizing the role of development in evolution into a coherent and productive synthesis, often called evo-devo. Evo-devo is seen as a replacement or amendment of the modern synthesis that has dominated the field of evolution since the 1940s and which, as even its architects confessed, was fundamentally incomplete because development remained outside its theoretical framework (Mayr and Provine 1980). As the volume attests, there is now a strong feeling that the time is ripe for the consolidation of evo-devo, and that the field is mature enough so that mapping the theoretical terrain and experimental approaches is both feasible and scientifically productive. Now is an appropriate time to try to weave the strands of reasoning leading to the developmental perspective and offer a synthesis.

Systems Thinking Versus Population Thinking: Genotype Integration and Chromosomal Organization 1930s–1950s

This article describes how empirical discoveries in the 1930s–1950s regarding population variation for chromosomal inversions affected Theodosius Dobzhansky and Richard Goldschmidt. A significant fraction of the empirical work I discuss was done by Dobzhansky and his coworkers; Goldschmidt was an astute interpreter, with strong and unusual commitments. I argue that both belong to a mechanistic tradition in genetics, concerned with the effects of chromosomal organization and systems on the inheritance patterns of species. Their different trajectories illustrate how scientists’ commitments affect how they interpret new evidence and adjust to it. Dobzhansky was moved to revised views about selection, while Goldschmidt moved his attention to different genetic phenomena. However different, there are significant connections between the two that enrich our understanding of their views. I focus on two: the role of developmental considerations in Dobzhansky’s thought and the role of neutrality and drift in Goldschmidt’s evolutionary account. Dobzhansky’s struggle with chromosomal variation is not solely about competing schools of thought within the selectionist camp, as insightfully articulated by John Beatty, but also a story of competition between selectionist thinking and developmental perspectives. In contraposition, Goldschmidt emphasized the role of low penetrance mutations that spread neutrally and pointed out that drift could result from developmental canalization. This account adds to the dominant story about Goldschmidt’s resistance to the splitting of development from genetics, as told by Garland Allen and Michael Dietrich. The story I tell illustrates how developmental thinking and genetic thinking conflicted and influenced researchers with different convictions about the significance of chromosomal organization.

Conceptual and Methodological Biases in Network Models

Many natural and biological phenomena can be depicted as networks. Theoretical and empirical analyses of networks have become prevalent. I discuss theoretical biases involved in the delineation of biological networks. The network perspective is shown to dissolve the distinction between regulatory architecture and regulatory state, consistent with the theoretical impossibility of distinguishing a priori between “program” and “data.” The evolutionary significance of the dynamics of trans‐generational and interorganism regulatory networks is explored and implications are presented for understanding the evolution of the biological categories development‐heredity, plasticity‐evolvability, and epigenetic‐genetic.