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Assimiliating an Associative Trait: from Eco-Physiology to Epigenetics

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Abstract

The possible evolutionary significance of epigenetic memory and codes is a key problem for extended evolutionary synthesis and biosemiotics. In this paper, some less known original works are reviewed which highlight theoretical parallels between current evolutionary epigenetics, on the one hand, and its predecessors in the eco-physiology of higher nervous activity, on the other. Recently, these areas have begun to converge, with first evidence now indicating the possibility of transgenerational epigenetic inheritance of conditional associations in the mammalian nervous system, and related findings in other taxa. This can serve as an interesting example of evolutionary code-making, where the molecular mechanisms underlying arbitrary associations between stimuli involve lasting changes in gene expression that may be transmitted epigenetically across generations, and which in some cases could be further assimilated into the genome over subsequent evolution. Although preliminary, such epigenetic scenarios would also offer an interesting, if so far overlooked parallel to earlier research carried out by one of I.P. Pavlov’s leading students, acad. P.K. Anokhin, and his colleagues, but also by eminent eco-physiologists of the time, several of whom offered arguments for the possibility of unconditional reflexes representing evolutionarily later, specialized, and reduced forms of associative reflexes, from which they may be derived. Although discarded under the growing dominance of modern synthesis, these early epigenetic investigations may deserve renewed attention in the modern context, and if further confirmed, could open essentially new perspectives on the morphofunctional evolution of the nervous system.

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Notes

  1. Cf. also Graham (2016), for historical and social contexts involved.

  2. In the latter case, the term “Baldwin effect” is often used, and more specific in emphasizing the initial behavioral component as the leading one in subsequent selection and retention (Baldwin 1896; Diogo 2017). However, there seems to be some controversy in the literature over whether the Baldwin effect would imply the phenotypic fixation and stabilization of a trait, i.e. its genetic assimilation, or should instead be restricted to those cases of genetic accommodation where more plastic phenotypes and responses are instead favored (Crispo 2007) – to be possibly followed by a separate process of trait fixation (through epigenetic mechanisms, or possibly, stochastic mutations in the same or competing traits). Here, the main interest lies with transgenerational epigenetics and genetic assimilation, thus not discussing the Baldwin effect as understood by Crispo (2007); however, the concepts remain variously employed and understood in their specifics.

  3. As the authors show in detail (Ginsburg and Jablonka 2010), the function of epigenetic control and silencing mechanisms, such as DNA methylation and ncRNA-mediated silencing in suppressing transposition, the growing evidence for the involvement of TEs in generating new genes, regulators, and new types of ncRNAs, and the sensitivity of the epigenetic mechanisms to stress, together support the conclusion that evolutionary diversification may be rapidly accelerated by stressful conditions (Ginsburg and Jablonka 2010).

  4. Interestingly, spectrometric analysis of this complex natural stimulus showed that it consists of sounds ranging from 0,1–8 kHz. However, the effective frequencies evoking the elimentary reaction (0,12–1,2 kHz) lay in the foremost part of the maternal “kr-r-r-r“sound spectrum, showing it produces an anticipatory and heterochronic receptor response in the nestlings (i.e., a temporally segmented signaling response) (Milyagin 1954).

  5. It’s important to note that this was not an artificial selection experiment, but an evolutionary behavioral one, where the learning constraints biased in favor of particular association types emerged spontaneously across generations, in response to the correspondingly structured environmetal correlations in the lineages. Although the study used only behavioral, not (epi)genomic or neurobiological measures, it nonetheless demonstrates how basic and longstanding problems can be tractable via relatively simple and accessible experimental designs. Indeed, such evolution of learning ability could probably seen as a fundamental, if much overlooked aspect of the evolution of development more generally (or developmental evolution), as approached in the frameworks of evo-devo and EES. Related problems are briefly mentioned below and in the discussion, also with respect to the limitations of learning theory.

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Acknowledgements

This work has been supported by Charles University Grant Agency grant no 926916. The author would like to thank an anonymous reviewer for extensive comments on an early version of this paper.

Conflict of Interest: The author declares no conflict of interest.

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    Andres Kurismaa

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Kurismaa, A. Assimiliating an Associative Trait: from Eco-Physiology to Epigenetics. Biosemiotics 11, 199–229 (2018). https://doi.org/10.1007/s12304-018-9324-0

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