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Is Non-genetic Inheritance Just a Proximate Mechanism? A Corroboration of the Extended Evolutionary Synthesis

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Abstract

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.

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Notes

  1. We note that while D&R attribute the distinction between general and specific evolutionary theories to Webb (2011), it is much older. Lewontin (1970), for example, clearly spelled out the general aspects of Darwinian evolution (variation, inheritance, and differential fitness), and explained how genetic evolution is but one specific theory that fulfills these criteria. It is curious that Webb (2011) cites no references in his paper, neither Lewontin (1970) nor any of the large subsequent literature that has built on Lewontin’s distinction.

  2. Natural selection can also act on cultural or epigenetic variation, such as when differential birth rates affect the spread of different religions (Hout et al. 2001), or epigenetic variants that promote tameness are selected during domestication, as suggested by artificial selection experiments in silver foxes (Jablonka and Raz 2009).

  3. Dickins and Barton (in press) maintain that all such cultural dynamics (such as language change) should be seen as proximate rather than ultimate causes. They equate cultural evolution with “historical accounts,” which “are not in any sense default ultimate accounts,” because (1) historical/cultural dynamics are governed by ultimate genetic causes at some higher level of organization, and (2) there is no adequately worked-out theory of cultural evolution that provides an equivalent level of explanatory power to genetic evolution. We disagree. Regarding point (2), decades of empirical and theoretical work in cultural evolution has identified numerous learning biases that can explain specific behavioral patterns (Mesoudi 2011; Richerson and Boyd 2005), including frequency-dependent (e.g., conformist or anti-conformist) biases and model-based biases such as prestige or success bias. Regarding point (1), as we argued above, the fact that cultural learning biases may have a genetic origin does not imply that the behavior that results from cultural dynamics is under direct genetic control. Hence our claim that these cultural dynamics are often more appropriately seen as ultimate, rather than (or as well as) proximate, causes of behavior.

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Authors and Affiliations

  1. Department of Anthropology, Durham University, Durham, UK

    Alex Mesoudi

  2. CNRS; Station d’Écologie Expérimentale du CNRS à Moulis, 09200, Moulis, France

    Simon Blanchet

  3. EDB (Laboratoire Évolution & Diversité Biologique), CNRS, UPS, ENFA, UMR 5174, 31062, Toulouse, France

    Simon Blanchet, Étienne Danchin & Benoît Pujol

  4. CNRS; Centre d’Écologie Fonctionnelle et Évolutive, UMR 5175, Montpellier, France

    Anne Charmantier

  5. Department of Biology, Stanford University, Stanford, CA, USA

    Laurel Fogarty

  6. The Cohn Institute for the History and Philosophy of Science and Ideas, Tel-Aviv University, Tel-Aviv, Israel

    Eva Jablonka

  7. School of Biology, University of St. Andrews, St. Andrews, Fife, Scotland, UK

    Kevin N. Laland & Thomas J. H. Morgan

  8. Department of Theoretical Biology, University of Vienna, Vienna, Austria

    Gerd B. Müller

  9. Mansfield College, University of Oxford, Oxford, UK

    F. John Odling-Smee

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  1. Alex Mesoudi
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  3. Anne Charmantier
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  7. Kevin N. Laland
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  8. Thomas J. H. Morgan
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  11. Benoît Pujol
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Correspondence to Alex Mesoudi.

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Mesoudi, A., Blanchet, S., Charmantier, A. et al. Is Non-genetic Inheritance Just a Proximate Mechanism? A Corroboration of the Extended Evolutionary Synthesis. Biol Theory 7, 189–195 (2013). https://doi.org/10.1007/s13752-013-0091-5

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