Abstract
In this paper, we adopt a physiological perspective in order to produce an intelligible overview of biological transmission in all its diversity. This allows us to put forward the analysis of transmission mechanisms, with the aim of complementing the usual focus on transmitted factors. We underline the importance of the structural, dynamical, and functional features of transmission mechanisms throughout organisms’ life cycles in order to answer to the question of what is passed on across generations, how and why. On this basis, we propose a vision of biological transmission as networks of heterogeneous physiological mechanisms, not restricted to transmission mechanisms stricto sensu. They prove to be themselves suited candidates for evolutionary explanations. They are processes both necessary for evolution to happen and resulting themselves from evolution. This leads us to call for a strategy of endogenization to account for transmission, and more specifically inheritance, as evolved and evolving physiological mechanisms.
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Notes
There are some exceptions, for instance Mossio and Pontarotti’s (2019) account of heredity which is based on an organizational perspective.
In a previous paper (Merlin and Riboli-Sasco 2017), we introduced three pairs of criteria (channel 1/channel 2, durability/residency, selectively relevant/neutral stable factor) in order to map different forms of transmission in terms of their architecture and their dynamics. However, our objective was only partially met, in particular due to the under characterization of transmission mechanisms. We seek to remedy this shortcoming here.
In Okasha’s words, the “strategy of endogenization” in evolutionary biology “involves devising evolutionary explanations for biological features that were originally part of the background conditions, or scaffolding, against which such explanations took place. Where successful, the features in question cease to be part of the background and are brought within the fold of evolutionary theory, or endogenized” (2018: p. 2).
By “transmitted factors” we mean various sorts of entities, and the processes they implement, that are passed on between organisms (i.e., the content of transmission such as stretches of DNA sequences, biochemical products, ecological niches, cognitive patterns, or cultural items). We are not interested in their informative value, but rather by the way these factors are mechanistically handled by transmission mechanisms.
Thus, our view is completely different from, for instance, that of Gilbert (2014) who, from a holobiont perspective, stresses the relations of co-dependency between various organic components, and argues for birth as the origin of a new interacting community composed by the eukaryotic body and its symbiotic microbes.
The transmission of language is a telling example of why mechanisms should receive more attention in the study of transmission. When the pattern traced by language transmission is examined, one is likely to find a network whose structure is close to a binary tree. Indeed, language is generally passed vertically, from parents to offspring. On this basis (that is, from a simple examination of the pattern of language transmission) one could infer that language is passed on through channel 1. One could even come to the conclusion that it is genetically transmitted. The only way one could discover that, on the contrary, language is transmitted via channel 2 (that is, by family learning) is by examining the mechanisms involved in its transfer—generally speaking, a transmission from parents to offspring.
Note that we consider transmission in mechanist terms, firstly because of the widespread use of mechanism-talk in biology, and in particular as regards the molecular and the cellular levels, and secondly because we consider that a mechanistic perspective rather than a causal non-mechanist perspective can allow a fine-grained identification of the transmission-related elements (that is, the entities and activities) that either require further investigation or have not yet been studied. A non-mechanist causal perspective might overlook certain aspects of the phenomenon of transmission as it is concerned with a more coarse-grained level.
By “transmission stricto sensu” we mean the act of transferring something by one organism to another (a pre-existing or a new one).
There are two reasons why this sort of transmission blocking mechanism has tended to be overlooked. First, the prevalent focus on transmitted factors has neglected the study of transmission mechanisms and, particularly, of mechanisms partially or completely blocking transmission. Second, any investigation of this kind of mechanism is faced with an important experimental barrier due to the fact that it attempts to study what potentially could be or could have been passed on, rather than what is actually transmitted. We thank one anonymous referee for raising this point.
As remarked by one anonymous referee, our view of transmission mechanisms raises the question of their spatiotemporal boundaries and of how they can be distinguished from developmental mechanisms. First, even though active transmission mechanisms can be found at any stage of a lifecycle, each mechanism has definite spatiotemporal boundaries determined by the phases of activity of its component entities. Second, transmission and developmental mechanisms are both physiological mechanisms. Thus, they do indeed overlap (think, for instance, of DNA replication, segregation of the germ-line, epigenome reprogramming, etc., but also of various social interactions that contribute both to cultural transmission and to brain development). However, they do not merge. For instance, mechanisms involved in morphogenesis (cell differentiation, cell contraction, cell migration, etc.) are not transmission mechanisms, even though they can depend on them (e.g., cell differentiation depends, among other mechanisms, on the mechanism of epigenetic reprogramming and is related to the mechanism of cell division allowing a cell type to be maintained through a cellular lineage). We thank the anonymous referee for raising these two questions.
For a soundly-argued defense of the shift toward a network-based conception in the study of all levels of biological organization, see Bapteste and Huneman (2018).
Skinner (2008) rightly specifies that, in the case of gestating females, F3 is the first generation to be considered when determining whether some transgenerational phenotype is due to transmission or to environmental exposure. Thus, the F3 generation is indeed the first not to be directly exposed to the same environment as the gestating mother (F0) during embryogenesis.
Actually, Bourrat (2013) uses the term “heredity” in his paper. However, his definition is in line with our definition of “inheritance”. This is why, in order to avoid any confusion, we keep to our own terminology.
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Acknowledgements
We would thank for their contributions and feedback the three anonymous reviewers and our collaborators Lucie Laplane, Laurent Loison, Antonine Nicoglou, Leïla Perié, Arnaud Pocheville, Gaëlle Pontarotti, and Guillaume Achaz. Beyond our research community, we would also thank colleagues, friends, and family who have read and discussed this work with us.
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Merlin, F., Riboli-Sasco, L. Inheritance as Evolved and Evolving Physiological Processes. Acta Biotheor 69, 417–433 (2021). https://doi.org/10.1007/s10441-020-09396-7
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DOI: https://doi.org/10.1007/s10441-020-09396-7