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Modern evolutionary biology is founded on the Mendelian-genetic model of inheritance, but it is now clear that this model is incomplete. Empirical evidence shows that environment (encompassing all external influences on the genome) can impose transgenerational effects and generate heritable variation for a broad array of traits in animals, plants, and other organisms. Such effects can be mediated by the transmission of epigenetic, cytoplasmic, somatic, nutritional, environmental, and behavioral variation. Building on the work of many authors, we outline a general framework for conceptualizing nongenetic inheritance and its evolutionary implications. This framework shows that, by decoupling phenotypic change from the genotype, nongenetic inheritance can circumvent the limitations of genetic inheritance and thereby influence population dynamics and alter the fitness landscape. The weight of theory and empirical evidence indicates that nongenetic inheritance is a potent factor in evolution that can engender outcomes unanticipated under the Mendelian-genetic model.

Neo-Darwinian evolutionary theory is based on exquisite selection of phenotypes caused by small genetic variations, which is the basis of quantitative trait contribution to phenotype and disease. Epigenetics is the study of nonsequence-based changes, such as DNA methylation, heritable during cell division. Previous attempts to incorporate epigenetics into evolutionary thinking have focused on Lamarckian inheritance, that is, environmentally directed epigenetic changes. Here, we propose a new non-Lamarckian theory for a role of epigenetics in evolution. We suggest that genetic variants that do not change the mean phenotype could change the variability of phenotype; and this could be mediated epigenetically. This inherited stochastic variation model would provide a mechanism to explain an epigenetic role of developmental biology in selectable phenotypic variation, as well as the largely unexplained heritable genetic variation underlying common complex disease. We provide two experimental results as proof of principle. The first result is direct evidence for stochastic epigenetic variation, identifying highly variably DNA-methylated regions in mouse and human liver and mouse brain, associated with development and morphogenesis. The second is a heritable genetic mechanism for variable methylation, namely the loss or gain of CpG dinucleotides over evolutionary time. Finally, we model genetically inherited stochastic variation in evolution, showing that it provides a powerful mechanism for evolutionary adaptation in changing environments that can be mediated epigenetically. These data suggest that genetically inherited propensity to phenotypic variability, even with no change in the mean phenotype, substantially increases fitness while increasing the disease susceptibility of a population with a changing environment.

This review describes new developments in the study of transgenerational epigenetic inheritance, a component of epigenetics. We start by examining the basic concepts of the field and the mechanisms that underlie epigenetic inheritance. We present a comprehensive review of transgenerational cellular epigenetic inheritance among different taxa in the form of a table, and discuss the data contained therein. The analysis of these data shows that epigenetic inheritance is ubiquitous and suggests lines of research that go beyond present approaches to the subject. We conclude by exploring some of the consequences of epigenetic inheritance for the study of evolution, while also pointing to the importance of recognizing and understanding epigenetic inheritance for practical and theoretical issues in biology.

The aim of this article is to put the growing interest in epigenetics in the field of evolutionary theory into a historical context. First, I assess the view that epigenetic inheritance could be seen as vindicating a revival of (neo)Lamarckism. Drawing on Jablonka's and Lamb's considerable output, I identify several differences between modern epigenetics and what Lamarckism was in the history of science. Even if Lamarckism is not back, epigenetic inheritance might be appealing for evolutionary biologists because it could potentiate two neglected mechanisms: the Baldwin effect and genetic assimilation. Second, I go back to the first ideas about the Baldwin effect developed in the late nineteenth century to show that the efficiency of this mechanism was already linked with a form of non-genetic inheritance. The opposition to all forms of non-genetic inheritance that prevailed at the time of the rise of the Modern Synthesis helps to explain why the Baldwin effect was understood as an insignificant mechanism during the second half of the twentieth century. Based on this historical reconstruction, in §4, I examine what modern epigenetics can bring to the picture and under what conditions epigenetic inheritance might be seen as strengthening the causal relationship between adaptability and adaptation. Throughout I support the view that the Baldwin effect and genetic assimilation, even if they are quite close, should not be conflated, and that drawing a line between these concepts is helpful in order to better understand where epigenetic inheritance might endorse a new causal role. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'

In recent years, a number of researchers have advocated extending the modern synthesis in evolutionary biology. One of the core arguments made in favour of an extension comes from work on soft inheritance systems, including transgenerational epigenetic effects, cultural transmission and niche construction. In this study, we outline this claim and then take issue with it. We argue that the focus on soft inheritance has led to a conflation of proximate and ultimate causation, which has in turn obscured key questions about biological organization and calibration across the life span to maximize average lifetime inclusive fitness. We illustrate this by presenting hypotheses that we believe incorporate the core phenomena of soft inheritance and will aid in understanding them.

The inheritance of characteristics induced by the environment has often been opposed to the theory of evolution by natural selection. However, although evolution by natural selection requires new heritable traits to be produced and transmitted, it does not prescribe, per se, the mechanisms by which this is operated. The mechanisms of inheritance are not, however, unconstrained, because they are themselves subject to natural selection. We introduce a schematic, analytically solvable mathematical model to compare the adaptive value of different schemes of inheritance. Our model allows for variations to be inherited, randomly produced, or environmentally induced, and, irrespectively, to be either transmitted or not during reproduction. The adaptation of the different schemes for processing variations is quantified for a range of fluctuating environments, following an approach that links quantitative genetics with stochastic control theory.

We present a very general model of epigenetic evolution unifying (neo-)Darwinian and (neo-)Lamarckian viewpoints. The evolution is represented in the form of adaptive dynamics given by the quantum(-like) master equation. This equation describes development of the information state of epigenome under the pressure of an environment. We use the formalism of quantum mechanics in the purely operational framework. (Hence, our model has no direct relation to quantum physical processes inside a cell.) Thus our model is about probabilities for observations which can be done on epigenomes and it does not provide a detailed description of cellular processes. Usage of the operational approach provides a possibility to describe by one model all known types of cellular epigenetic inheritance.

There’s something strange about Freud’s Civilization and its Discontents (1930). Biologically, Freud was a Neo-Lamarckian, who believed in both the modification of organisms through need and the inheritance of acquired characteristics. However, in Civilization, Freud argued that because human nature is immutable, society has dim odds of improving substantially. Lamarckians, of course, rejected that any species-nature is immutable, as species can always be transformed via the inheritance of acquired characteristics. In fact, many of Freud’s Viennese contemporaries—such as Wilhelm Reich, Julius Tandler, and Paul Kammerer—took their Lamarckism to license precisely the sorts of radical social projects Freud deemed impossible. Thus the Freud of Civilization helped himself to a rigid view of human nature which, given his associated biological views, he seemingly ought to have rejected. In this paper, I explain this apparent inconsistency, and suggest Freud resolved it in the following way: Freud was not merely a Lamarckian, but also a strong and peculiar kind of recapitulationist, who believed stages of psychological development both recapitulate phylogeny, and “remain with us” throughout both individual lives and future species-history. I suggest Freud’s recapitulationism supposed a certain inertia: what occurred in phylogenetic history cannot un-occur, and therefore there are aspects of our nature which we cannot un-acquire. In this way, Freud reached a rigid conception of human nature despite his Lamarckism.

This article considers the doctrine of energetical vitalism as proposed by the early twentieth-century philosopher, Eugenio Rignano. Rignano’s energetical vitalism aimed to present a comprehensive biological theory, addressing distinct phenomena of purposiveness—or what are called teleological phenomena—exclusive to the organic domain. His doctrine pivoted on two key hypotheses. The first, the hypothesis of vital energy, posited that life’s distinctiveness emanates from a unique energy form he termed “vital (or nervous) energy.” Rignano believed that while this form of energy shares attributes with conventional energy forms and adheres to basic laws of energetics, its manifestations are exclusively organic, dictating specific purposive phenomena. The second hypothesis, termed “centroepigenetic,” asserted that vital energies primarily accumulate in the chromosomes within nuclei but can be transferred through intercellular bridges connecting germinal and somatic nuclei. Rignano’s energetical vitalism synthesized ideas from three significant scientific trends of his era: the energetics, neo-Lamarckian, and mnemic movements. In closing, this article critiques Rignano’s energetical vitalism with two primary assertions. First, while empirical support for the vital energy hypothesis remains elusive, vitalism’s historical significance is arguably more profound than contemporary physicalists recognize, and it remains logically defensible to propose vitalistic hypotheses, irrespective of physicalist metaphysical constraints. Second, Rignano’s centroepigenetic hypothesis can be seen as prescient in light of recent molecular genetic discoveries. These two points are informed by Hasok Chang’s perspectives on “outdated” scientific theories.

The consensus regarding quantum measurements rests on two statements: (i) von Neumann’s standard quantum measurement theory leaves undetermined the basis in which observables are measured, and (ii) the environmental decoherence of the measuring device (the “meter”) unambiguously determines the measuring (“pointer”) basis. The latter statement means that the environment monitors (measures) selected observables of the meter and (indirectly) of the system. Equivalently, a measured quantum state must end up in one of the “pointer states” that persist in the presence of the environment. We find that, unless we restrict ourselves to projective measurements, decoherence does not necessarily determine the pointer basis of the meter. Namely, generalized measurements commonly allow the observer to choose from a multitude of alternative pointer bases that provide the same information on the observables, regardless of decoherence. By contrast, the measured observable does not depend on the pointer basis, whether in the presence or in the absence of decoherence. These results grant further support to our notion of Quantum Lamarckism, whereby the observer’s choices play an indispensable role in quantum mechanics.