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Mapping Biological Transmission: An Empirical, Dynamical, and Evolutionary Approach

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Abstract

The current debate over extending inheritance and its evolutionary impact has focused on adding new categories of non-genetic factors to the classical transmission of DNA, and on trying to redefine inheritance. Transmitted factors have been mainly characterized by their directions of transmission (vertical, horizontal, or both) and the way they store variations. In this paper, we leave aside the issue of defining inheritance. We rather try to build an evolutionary conceptual framework that allows for tracing most, if not all forms of transmission and makes sense of their different tempos and modes. We discuss three key distinctions that should in particular be the targets of theoretical and empirical investigation, and try to assess the interplay among them and evolutionary dynamics. We distinguish two channels of transmission (channel 1 and channel 2), two measurements of the temporal dynamics of transmission, respectively across and within generations (durability and residency), and two types of transmitted factors according to their evolutionary relevance (selectively relevant and neutral stable factors). By implementing these three distinctions we can then map different forms of transmission over a continuous space describing the combination of their varying dynamical features. While our aim is not to provide yet another model of inheritance, putting together these distinctions and crossing them, we manage to offer an inclusive conceptual framework of transmission, grounded in empirical observation, and coherent with evolutionary theory. This interestingly opens possibilities for qualitative and quantitative analyses, and is a necessary step, we argue, in order to question the interplay between the dynamics of evolution and the dynamics of multiple forms of transmission.

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Notes

  1. By factor we intend various sorts of physical entities and processes that are mechanistically transmitted and are involved in biological processes.

  2. In this paper, we thus pay attention as much as possible not to use the term « inheritance » .

  3. The more general issue of how to (re)define the notion of inheritance follows from these questions; however, as stated above, it will not be addressed in this paper.

  4. In organisms with sexual reproduction, transmission via channel 1 involves the passage through a unicellular bottleneck associated with a specific type of cellular division: meiosis. Gametes are produced by meiosis and their fusion is the starting point of the development of the new organism. Transmission via bottleneck is a special, relatively frequent, case of transmission via channel 1: it is an evolved mechanism of transmission for a “fresh start” and is coupled with a developmental process. This specific feature of sexual reproduction perfectly fits the idea that factors transmitted through channel 1 travel from cell to cell directly, i.e., through a chain of cell divisions and fusions.

  5. Even though material overlap does not prove to be a necessary feature for the transmission of something, it could be considered a guarantee of a more faithful transmission. This faithfulness is the consequence of the stability of the matter that is actually transmitted. We can think about the difference between written and oral transmission in an analogous way, with the example of a printed book and an oral (non-recorded) discourse: the former (imagine the book passed on to many people and read) is likely to be much more precise and faithful than the oral discourse after an equivalent number of people have repeated it.

  6. As suggested by an anonymous referee, we see a major ontological difference between a hormone passed via cellular reproduction (in the egg yolk) and the same hormone being transmitted via the placenta: they differ in the transmission mechanisms involved. In the first case, this channel 1 type of transmission happens because of cell division (i.e., when the cytoplasmic content splits), and so only requires the availability and distribution of the hormone while the mechanism is taking place; whereas in the latter case, which we classify as a channel 2 transmission and in which the hormone is passed on through blood, the evolution of other complex structures with specific functions, such as the placenta, is required.

  7. For a review of epigenetic mechanisms involved in behavioural transmission in the specific case of maternal care, see Champagne (2008); see also Richardson et al. (2014).

  8. We specifically talk about the durability of a factor and not about the durability of its effect, the latter being more likely to have a shorter durability due to the inherent variability of the implementation of a factor into an effect (or, for genetics, the expression of a trait) and to the variability resulting from changes in the environment.

  9. In principle, residency is also a measurement of the timing of transmission, i.e., it should allow for identifying when a factor is acquired during the life cycle of an individual organism and when it is lost; but these two points in time are in most cases very difficult to measure.

  10. Selectively relevant factors are those that are actually considered to be heritable difference makers for which a measurement of heritability can be estimated, defined as a proportion of variance due to certain transmitted factors (i.e., genes according to the traditional gene-centered view of evolution; more factors, and not just genes, according to a broader, inclusive, conception of inheritance, e.g., Danchin et al. 2011). However, in this paper we do not think that transmitted factors are necessarily difference makers. Our present analysis covers all factors that are passed on from one organism to another by various transmission mechanisms, regardless of their selective value.

  11. This means that the maintenance of some factor does not necessarily depend on the presence of standing variation in the population, so that factors that are important for the inheritance of some trait are functional and transmitted even though they are not variable. As suggested by an anonymous referee, this point relates to Mameli’s distinction between the inheritance of features (inheritanceF) and the inheritance of variation (inheritanceV); see Mameli 2005.

  12. Note that high durability (longevity through descent, in Dawkins’ terms) has been a typical feature of replicators since Hull’s and Dawkins’ conceptions (Hull 1980; Dawkins 1982), and up until the concept of the extended replicator (Sterelny et al. 1996).

  13. Shea et al. (2011) point to some related differences between epigenetic inheritance in plants and in animals. They express these in terms of their distinction between “selection-based” and “detection-based” epigenetic effects. Even though they can rely on the same epigenetic mechanisms (e.g., DNA methylation), these two types of effects have different functions: selection-based effects “carry adaptive information in virtue of selection over many generations of reliable transmission”, and detection-based effects “carry information about an environmental feature detected by the parent” (p. 8). Shea et al. suggest that, because of developmental reasons linked to the germ line-soma separation, detection-based effects may be less common in animals than in plants. Moreover, for selective reasons linked to the motility of animals and the fact that they have a nervous system, animals may have less need of epigenetic inheritance than plants. Finally, Shea et al. also suggest that, because of the extensive reprogramming of the epigenome in animals, long-term reliable transmission of epigenetic variants (i.e., high durability, in our terms), and so selection-based effects, will be rare. Thus, selection-based effects would, in our framework, be factors transmitted with high durability while detection-based effects display low durability. Still, both are evolutionary meaningful and the difference in transmission mechanisms in both cases results from selection.

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Acknowledgments

We would like to thank the people of the Institut d’histoire et de philosophie des sciences et des techniques (Paris) belonging to the ANR project “ExplaBio”, in particular Philippe Huneman, as well as the anonymous referees for helpful objections and remarks.

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Authors and Affiliations

  1. IHPST – CNRS & Université Paris 1 Panthéon-Sorbonne, 13 rue du Four, 75006, Paris, France

    Francesca Merlin

  2. Atelier des Jours à Venir, 97 allée Théodore Monod, 64210, Bidart, France

    Livio Riboli-Sasco

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  1. Francesca Merlin
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Correspondence to Francesca Merlin.

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Merlin, F., Riboli-Sasco, L. Mapping Biological Transmission: An Empirical, Dynamical, and Evolutionary Approach. Acta Biotheor 65, 97–115 (2017). https://doi.org/10.1007/s10441-017-9305-8

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