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Etienne Danchin - One of the best experts on this subject based on the ideXlab platform.
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EpiGenetically facilitated mutational assimilation: epiGenetics as a hub within the inclusive evolutionary synthesis
Biological Reviews, 2019Co-Authors: Etienne Danchin, Benoit Pujol, Arnaud Pocheville, Olivier Rey, Simon BlanchetAbstract:After decades of debate about the existence of non‐Genetic Inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐Genetic and Genetic Inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐Genetic Inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie Inheritance. We then review several lines of argument for the existence of interactions between non‐Genetic and Genetic components of Inheritance, leading to a discussion of the contrasting timescales of action of non‐Genetic and Genetic Inheritance. This raises the question of how the fidelity of the Inheritance system can match the rate of environmental variation. This question is central to understanding the role of different Inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from Inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking Genetic and non‐Genetic Inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the Inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐Genetic information converge towards epiGenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epiGenetic marks as potentially generating a final shift from epiGenetic to Genetic encoding. This sequence of shifts suggests the existence of a relay in Inheritance systems from relatively labile ones to gradually more persistent modes of Inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of Genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the Genetic assimilation relay proposed here lies in the fact that a given form of Inheritance can affect the rate of change of other Inheritance systems. To explore the consequences of such inter‐connection among Inheritance systems, we briefly review published theoretical models to build a model of Genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among Inheritance systems has the potential to generate a form of Genetic assimilation. In this hypothesis, epiGenetics appears as a hub by which non‐Genetically inherited environmentally induced variation in traits can become Genetically encoded over generations, in a form of epiGenetically facilitated mutational assimilation. Finally, we illustrate some of the major implications of our hypothetical framework, concerning mutation randomness, the central dogma of molecular biology, concepts of Inheritance and the curing of inherited disorders, as well as for the emergence of the inclusive evolutionary synthesis.
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The Double Pedigree: A Method for Studying Culturally and Genetically Inherited Behavior in Tandem
PLoS ONE, 2013Co-Authors: Etienne Danchin, Benoit Pujol, Richard WagnerAbstract:Transgenerational sources of biological variation have been at the center of evolutionary studies ever since Darwin and Wallace identified natural selection. This is because evolution can only operate on traits whose variation is transmitted, i.e. traits that are heritable. The discovery of Genetic Inheritance has led to a semantic shift, resulting in the tendency to consider that only genes are inherited across generations. Today, however, concepts of heredity are being broadened again to integrate the accruing evidence of non-Genetic Inheritance, and many evolutionary biologists are calling for the inclusion of non-Genetic Inheritance into an inclusive evolutionary synthesis. Here, we focus on social heredity and its role in the Inheritance of behavioral traits. We discuss quantitative Genetics methods that might allow us to disentangle Genetic and non-Genetic transmission in natural populations with known pedigrees. We then propose an experimental design based on cross-fostering among animal cultures, environments and families that has the potential to partition inherited phenotypic variation into socially (i.e. culturally) and Genetically inherited components. This approach builds towards a new conceptual framework based on the use of an extended version of the animal model of quantitative Genetics to integrate Genetic and cultural components of behavioral Inheritance. Citation: Danchin E, Pujol B, Wagner RH (2013) The Double Pedigree: A Method for Studying Culturally and Genetically Inherited Behavior in Tandem. PLoS ONE 8(5): e61254.
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The double pedigree: a method for studying culturally and Genetically inherited behavior in tandem.
PloS one, 2013Co-Authors: Etienne Danchin, Benoit Pujol, Richard H. WagnerAbstract:Transgenerational sources of biological variation have been at the center of evolutionary studies ever since Darwin and Wallace identified natural selection. This is because evolution can only operate on traits whose variation is transmitted, i.e. traits that are heritable. The discovery of Genetic Inheritance has led to a semantic shift, resulting in the tendency to consider that only genes are inherited across generations. Today, however, concepts of heredity are being broadened again to integrate the accruing evidence of non-Genetic Inheritance, and many evolutionary biologists are calling for the inclusion of non-Genetic Inheritance into an inclusive evolutionary synthesis. Here, we focus on social heredity and its role in the Inheritance of behavioral traits. We discuss quantitative Genetics methods that might allow us to disentangle Genetic and non-Genetic transmission in natural populations with known pedigrees. We then propose an experimental design based on cross-fostering among animal cultures, environments and families that has the potential to partition inherited phenotypic variation into socially (i.e. culturally) and Genetically inherited components. This approach builds towards a new conceptual framework based on the use of an extended version of the animal model of quantitative Genetics to integrate Genetic and cultural components of behavioral Inheritance.
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Is Non-Genetic Inheritance Just a Proximate Mechanism? A Corroboration of the Extended Evolutionary Synthesis
Biological Theory, 2013Co-Authors: Alex Mesoudi, Laurel Fogarty, Thomas J. H. Morgan, Anne Charmantier, Eva Jablonka, Etienne Danchin, Gerd B. Müller, Simon Blanchet, Kevin N. Laland, F. John Odling-smeeAbstract:What role does non-Genetic Inheritance play in evolution? In recent work we have independently and collectively argued that the existence and scope of non-Genetic Inheritance systems, including epiGenetic Inheritance, niche construction/ecological Inheritance, and cultural Inheritance—alongside certain other theory revisions—necessitates an extension to the neo-Darwinian Modern Synthesis (MS) in the form of an Extended Evolutionary Synthesis (EES). However, this argument has been challenged on the grounds that non-Genetic Inheritance systems are exclusively proximate mechanisms that serve the ultimate function of calibrating organisms to stochastic environments. In this paper we defend our claims, pointing out that critics of the EES (1) conflate non-Genetic Inheritance with early 20th-century notions of soft Inheritance; (2) misunderstand the nature of the EES in relation to the MS; (3) confuse individual phenotypic plasticity with trans-generational non-Genetic Inheritance; (4) fail to address the extensive theoretical and empirical literature which shows that non-Genetic Inheritance can generate novel targets for selection, create new Genetic equilibria that would not exist in the absence of non-Genetic Inheritance, and generate phenotypic variation that is independent of Genetic variation; (5) artificially limit ultimate explanations for traits to gene-based selection, which is unsatisfactory for phenotypic traits that originate and spread via non-Genetic Inheritance systems; and (6) fail to provide an explanation for biological organization. We conclude by noting ways in which we feel that an overly gene-centric theory of evolution is hindering progress in biology and other sciences.
Franz J. Weissing - One of the best experts on this subject based on the ideXlab platform.
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Understanding 'Non-Genetic' Inheritance: Insights from Molecular-Evolutionary Crosstalk.
Trends in ecology & evolution, 2020Co-Authors: Irene Adrian-kalchhauser, Sonia E. Sultan, Lisa N S Shama, Helen Clare Spence-jones, Stefano Tiso, Claudia Isabelle Keller Valsecchi, Franz J. WeissingAbstract:Understanding the evolutionary and ecological roles of 'non-Genetic' Inheritance (NGI) is daunting due to the complexity and diversity of epiGenetic mechanisms. We draw on insights from molecular and evolutionary biology perspectives to identify three general features of 'non-Genetic' Inheritance systems: (i) they are functionally interdependent with, rather than separate from, DNA sequence; (ii) precise mechanisms vary phyloGenetically and operationally; and (iii) epiGenetic elements are probabilistic, interactive regulatory factors and not deterministic 'epialleles' with defined genomic locations and effects. We discuss each of these features and offer recommendations for future empirical and theoretical research that implements a unifying inherited gene regulation (IGR) approach to studies of 'non-Genetic' Inheritance.
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Understanding 'Non-Genetic' Inheritance: Insights from Molecular-Evolutionary Crosstalk
2020Co-Authors: Irene Adrian-kalchhauser, Sonia E. Sultan, Helen Clare Spence-jones, Stefano Tiso, Claudia Isabelle Keller Valsecchi, Lisa Shama, Franz J. WeissingAbstract:Understanding the evolutionary and ecological roles of 'non-Genetic' Inheritance is daunting due to the complexity and diversity of epiGenetic mechanisms. We draw on precise insights from molecular structures and events to identify three general features of 'non-Genetic' Inheritance systems that are central to broader investigations: (i) they are functionally interdependent with, rather than separate from, DNA sequence; (ii) each of these mechanisms is not uniform but instead varies phyloGenetically and operationally; and (iii) epiGenetic elements are probabilistic, interactive regulatory factors and not deterministic 'epi-alleles' with defined genomic locations and effects. We explain each feature and offer research recommendations. Finally, we consider existing evolutionary models for 'non-Genetic' Inheritance and present a new model that implements a unifying inherited gene regulation approach.
Tobias Uller - One of the best experts on this subject based on the ideXlab platform.
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Different perspectives on non-Genetic Inheritance illustrate the versatile utility of the Price equation in evolutionary biology.
Philosophical transactions of the Royal Society of London. Series B Biological sciences, 2020Co-Authors: Heikki Helanterä, Tobias UllerAbstract:The diversity of Genetic and non-Genetic processes that make offspring resemble their parents are increasingly well understood. In addition to Genetic Inheritance, parent-offspring similarity is affected by epiGenetic, behavioural and cultural mechanisms that collectively can be referred to as non-Genetic Inheritance. Given the generality of the Price equation as a description of evolutionary change, is it not surprising that the Price equation has been adopted to model the evolutionary implications of non-Genetic Inheritance. In this paper, we briefly introduce the heredity perspectives on which those models rely, discuss the extent to which these perspectives make different assumptions and place different emphases on the roles of heredity and development in evolution, and the types of empirical research programmes they motivate. The existence of multiple perspectives and explanatory aims highlight, on the one hand, the versatility of the Price equation and, on the other hand, the importance of understanding how heredity and development can be conceptualized in evolutionary studies. This article is part of the theme issue 'Fifty years of the Price equation'.
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The information value of non-Genetic Inheritance in plants and animals.
PloS one, 2015Co-Authors: Sinead English, Ido Pen, Nicholas Shea, Tobias UllerAbstract:Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epiGenetic states, nutrients, antibodies and hormones, and behavioural interactions after birth. While the evolutionary consequences of such non-Genetic Inheritance are increasingly well understood, less is known about how Inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-Genetic Inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to different inputs, including genes and non-Genetic factors transmitted from parents and the environment experienced during development. This framework shows how Genetic and non-Genetic Inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of Genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-Genetic Inheritance, as opposed to Genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-Genetic Inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-Genetic Inheritance depends on its mechanism, the pace of environmental change, and life history characteristics.
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Non-Genetic Inheritance and evolution
The Philosophy of Biology, 2013Co-Authors: Tobias UllerAbstract:Teaching evolution usually means an exclusive focus on transmission Genetics as the basis for heredity. The stability of DNA sequences gives the impression that the developmental history of individuals can be set aside and evolutionary change in phenotypes can be described as change in gene frequencies. This is the textbook version of evolution and the view that the majority of evolutionary biologists subscribe to. The unique position of DNA in heredity is now being challenged, however. Mounting empirical evidence suggests that phenotypic stability within lineages and differences between lineages can originate and be maintained via epiGenetic and behavioural mechanisms, even in the absence of Genetic variation. This raises questions regarding the evolutionary implications of such non-Genetic mechanisms of Inheritance, including whether they can bias the rate and direction of evolution or allow Inheritance of acquired characters. In this chapter, I outline the historical background to the development of the transmission Genetics view of heredity and how recent findings in molecular, developmental, and behavioural biology challenge the textbooks. I continue by showing how the heterogeneous cluster of non-Genetic mechanisms of Inheritance can contribute to an expanded version of evolutionary theory. Although it turns out that the special role played by genes in evolution can also be played by other Inheritance systems, the main conceptual advantage of recognizing non-Genetic mechanisms of Inheritance is that it stimulates an explicit consideration of developmental processes in evolutionary explanations. This helps us to connect the processes responsible for within-generation change (‘proximate questions’ or the domain of developmental biology) with among-generation change (‘ultimate question’ or the domain of evolutionary biology). Furthermore, it shows how the teaching of fundamental concepts in evolutionary biology can benefit from philosophical analysis informed by contemporary biological research.
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Integrating non-Genetic Inheritance in evolutionary theory. A primer
Non-Genetic Inheritance, 2013Co-Authors: Tobias Uller, Heikki HelanteräAbstract:Evolutionary biology traditionally equates Inheritance with transmission of genes from parents to offspring. However, recent literature calls for considering ‘non-Genetic Inheritance’ in evolutionary theory. These calls have met with substantial scepticism. What is more, they appear to have caused further confusion both with respect to what Inheritance is and what types of Inheritance mechanisms are evolutionarily consequential. Building on previous work, we make use of the Price Equation to outline a general discussion of how non-Genetic Inheritance can affect phenotypic change within populations, exemplified by epiGenetic Inheritance. This shows that integrating non-Genetic Inheritance in evolutionary theory will require specific attention to the developmental processes that shape the relationship between the fitness of parents and the phenotype of their offspring. (Less)
Irene Adrian-kalchhauser - One of the best experts on this subject based on the ideXlab platform.
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Understanding 'Non-Genetic' Inheritance: Insights from Molecular-Evolutionary Crosstalk.
Trends in ecology & evolution, 2020Co-Authors: Irene Adrian-kalchhauser, Sonia E. Sultan, Lisa N S Shama, Helen Clare Spence-jones, Stefano Tiso, Claudia Isabelle Keller Valsecchi, Franz J. WeissingAbstract:Understanding the evolutionary and ecological roles of 'non-Genetic' Inheritance (NGI) is daunting due to the complexity and diversity of epiGenetic mechanisms. We draw on insights from molecular and evolutionary biology perspectives to identify three general features of 'non-Genetic' Inheritance systems: (i) they are functionally interdependent with, rather than separate from, DNA sequence; (ii) precise mechanisms vary phyloGenetically and operationally; and (iii) epiGenetic elements are probabilistic, interactive regulatory factors and not deterministic 'epialleles' with defined genomic locations and effects. We discuss each of these features and offer recommendations for future empirical and theoretical research that implements a unifying inherited gene regulation (IGR) approach to studies of 'non-Genetic' Inheritance.
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Understanding 'Non-Genetic' Inheritance: Insights from Molecular-Evolutionary Crosstalk
2020Co-Authors: Irene Adrian-kalchhauser, Sonia E. Sultan, Helen Clare Spence-jones, Stefano Tiso, Claudia Isabelle Keller Valsecchi, Lisa Shama, Franz J. WeissingAbstract:Understanding the evolutionary and ecological roles of 'non-Genetic' Inheritance is daunting due to the complexity and diversity of epiGenetic mechanisms. We draw on precise insights from molecular structures and events to identify three general features of 'non-Genetic' Inheritance systems that are central to broader investigations: (i) they are functionally interdependent with, rather than separate from, DNA sequence; (ii) each of these mechanisms is not uniform but instead varies phyloGenetically and operationally; and (iii) epiGenetic elements are probabilistic, interactive regulatory factors and not deterministic 'epi-alleles' with defined genomic locations and effects. We explain each feature and offer research recommendations. Finally, we consider existing evolutionary models for 'non-Genetic' Inheritance and present a new model that implements a unifying inherited gene regulation approach.
Benoit Pujol - One of the best experts on this subject based on the ideXlab platform.
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EpiGenetically facilitated mutational assimilation: epiGenetics as a hub within the inclusive evolutionary synthesis
Biological Reviews, 2019Co-Authors: Etienne Danchin, Benoit Pujol, Arnaud Pocheville, Olivier Rey, Simon BlanchetAbstract:After decades of debate about the existence of non‐Genetic Inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐Genetic and Genetic Inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐Genetic Inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie Inheritance. We then review several lines of argument for the existence of interactions between non‐Genetic and Genetic components of Inheritance, leading to a discussion of the contrasting timescales of action of non‐Genetic and Genetic Inheritance. This raises the question of how the fidelity of the Inheritance system can match the rate of environmental variation. This question is central to understanding the role of different Inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from Inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking Genetic and non‐Genetic Inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the Inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐Genetic information converge towards epiGenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epiGenetic marks as potentially generating a final shift from epiGenetic to Genetic encoding. This sequence of shifts suggests the existence of a relay in Inheritance systems from relatively labile ones to gradually more persistent modes of Inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of Genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the Genetic assimilation relay proposed here lies in the fact that a given form of Inheritance can affect the rate of change of other Inheritance systems. To explore the consequences of such inter‐connection among Inheritance systems, we briefly review published theoretical models to build a model of Genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among Inheritance systems has the potential to generate a form of Genetic assimilation. In this hypothesis, epiGenetics appears as a hub by which non‐Genetically inherited environmentally induced variation in traits can become Genetically encoded over generations, in a form of epiGenetically facilitated mutational assimilation. Finally, we illustrate some of the major implications of our hypothetical framework, concerning mutation randomness, the central dogma of molecular biology, concepts of Inheritance and the curing of inherited disorders, as well as for the emergence of the inclusive evolutionary synthesis.
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The double pedigree: a method for studying culturally and Genetically inherited behavior in tandem.
PloS one, 2013Co-Authors: Etienne Danchin, Benoit Pujol, Richard H. WagnerAbstract:Transgenerational sources of biological variation have been at the center of evolutionary studies ever since Darwin and Wallace identified natural selection. This is because evolution can only operate on traits whose variation is transmitted, i.e. traits that are heritable. The discovery of Genetic Inheritance has led to a semantic shift, resulting in the tendency to consider that only genes are inherited across generations. Today, however, concepts of heredity are being broadened again to integrate the accruing evidence of non-Genetic Inheritance, and many evolutionary biologists are calling for the inclusion of non-Genetic Inheritance into an inclusive evolutionary synthesis. Here, we focus on social heredity and its role in the Inheritance of behavioral traits. We discuss quantitative Genetics methods that might allow us to disentangle Genetic and non-Genetic transmission in natural populations with known pedigrees. We then propose an experimental design based on cross-fostering among animal cultures, environments and families that has the potential to partition inherited phenotypic variation into socially (i.e. culturally) and Genetically inherited components. This approach builds towards a new conceptual framework based on the use of an extended version of the animal model of quantitative Genetics to integrate Genetic and cultural components of behavioral Inheritance.
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The Double Pedigree: A Method for Studying Culturally and Genetically Inherited Behavior in Tandem
PLoS ONE, 2013Co-Authors: Etienne Danchin, Benoit Pujol, Richard WagnerAbstract:Transgenerational sources of biological variation have been at the center of evolutionary studies ever since Darwin and Wallace identified natural selection. This is because evolution can only operate on traits whose variation is transmitted, i.e. traits that are heritable. The discovery of Genetic Inheritance has led to a semantic shift, resulting in the tendency to consider that only genes are inherited across generations. Today, however, concepts of heredity are being broadened again to integrate the accruing evidence of non-Genetic Inheritance, and many evolutionary biologists are calling for the inclusion of non-Genetic Inheritance into an inclusive evolutionary synthesis. Here, we focus on social heredity and its role in the Inheritance of behavioral traits. We discuss quantitative Genetics methods that might allow us to disentangle Genetic and non-Genetic transmission in natural populations with known pedigrees. We then propose an experimental design based on cross-fostering among animal cultures, environments and families that has the potential to partition inherited phenotypic variation into socially (i.e. culturally) and Genetically inherited components. This approach builds towards a new conceptual framework based on the use of an extended version of the animal model of quantitative Genetics to integrate Genetic and cultural components of behavioral Inheritance. Citation: Danchin E, Pujol B, Wagner RH (2013) The Double Pedigree: A Method for Studying Culturally and Genetically Inherited Behavior in Tandem. PLoS ONE 8(5): e61254.