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Environmental Inheritance: Conceptual Ambiguities and Theoretical Issues

  • Thematic Issue Article: Conceptualizing the Environment in Natural Sciences
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Abstract

The concept of biological inheritance has recently been extended so as to integrate, among other elements, parts of organisms’ environments. The literature refers to the trans-generational reconstruction of these parts in terms of environmental or ecological inheritance. This article’s main objective is to clarify the different meanings of "environmental inheritance," to underline so far unnoticed theoretical difficulties associated to this polysemous notion and to consequently argue that inheritance, even when extended, should be theoretically distinguished from trans-generational environmental stability. After disentangling the different meanings of environmental inheritance, I underline that studies dealing with this concept place themselves in the wake of earlier contributions about biological environment and elaborate on the role of organisms in the determination of their relevant developmental and selective surroundings. This leads me to question the legitimacy of the category shift operated by niche inheritance proponents—from environment to inheritance—and to explain why the very concept of inherited environment shows important and so far unnoticed theoretical limitations (theoretical redundancy and theoretical inconsistency). In this context, I assert the necessity to distinguish two related but different research programs: the construction of a finer-grained theory of environment and the elaboration of an extended theory of inheritance.

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Notes

  1. In this article, I will focus on the scale of organisms, which is the one usually considered in the literature about extended inheritance. However, the analysis provided here can be applied to different levels (cells, social groups, ecosystems).

  2. Biological environment stricto sensu is considered in opposition to environment at large (notably geographical). For more details, see the third section.

  3. Some authors have distinguished “heredity,” the reoccurrence of traits across generations, the pattern of parent–offspring resemblance, and “inheritance,” the process that underpins this phenomenon (see for example Bonduriansky 2012). In this article, I chose to use the word “inheritance” to refer to both elements. Accordingly, inheritance refers here to the reoccurrence of observable morphological, physiological, and behavioral traits and to the processes underpinning this reoccurrence. This choice is notably motivated by the fact that the literature generally talks about ecological or environmental “inheritance,” not “heredity.” In addition, in the case of nongenetic inheritance, it is sometimes hard to make a clear distinction between outcomes and underpinning processes, notably for behavioral transmission.

  4. In its adjectival form.

  5. The protein hypothesis was linked to the fact that genes were thought to be autocatalytic objects (Muller 1922), and that proteins had long been known for their catalytic properties.

  6. One spontaneously talks about nutrition in an environment, of development in an environment, but about inheritance of an environment. The question that I raise in this article is whether such difference is linked to the metaphorical origin of the concept of inheritance, and to its larger use beyond biology.

  7. “In the same way,” here, does not mean that genetic and environmental inheritance rely on the same mechanisms. It more simply refers to the idea that parts of the environment are, like genes, considered as components of biological legacies.

  8. To Dawkins (1976), the concept of "gene" specifically refers to a strand of DNA that is in competition for a locus across generations.

  9. Dawkins' and Turner’s approaches are dealing with evolutionary timescale but the inherited environments they put forward are not selective ones.

  10. The concept of extended phenotype does not have the same meaning in this context though. To Bonduriansky, it mainly refers to the transmission of elements of the parental environment.

  11. Darwin’s studies about earthworm modifications of the soil acknowledge that organisms can transform the environment in which they live. However, in The Formation of Vegetable Mould Through the Action of Worms, Darwin’s main concern is to assess the role of worms in the transformation of the earth. As a result, it differs from that of Lewontin and followers, which is to reject the idea according to which organisms are passive agents in development and evolution.

  12. The association between “functional” and “developmental” niche inheritance is not found in the literature. However, I consider that both refer to developmental timescale and therefore significantly overlap.

  13. In this article, I assume an equivalence between “ecological” and “niche” inheritance. However, this equivalence is not always endorsed by Odling-Smee (2010, p. 182).

  14. This analysis is qualified as epistemological insofar as it questions the constituents of scientific discourse, the theoretical concepts that are found in it.

  15. This theoretical heritage is not always explicit in the papers written by niche-inheritance proponents. For example, Stotz (2017) clearly refers to Lewontin’s work, and Odling-Smee (2010) mentions Waddington’s and Lewontin’s studies. However, none of them explicitly mention Canguilhem's or Uexkull's studies, in spite of striking echoes. In addition, the quotations of Waddington, Lewontin, and Canguilhem that I provide in this section show that the studies that inspired—more or less explicitly—niche-inheritance proponents were not about inheritance but about “environment” (or “milieu” for Canguilhem).

  16. Waddington and Lewontin did not discuss the problem of the transition between functional/developmental and selective environments. This problem will be addressed later in the article.

  17. In the same vein, Goldstein (1951, p. 76) considers that the environment is shaped as the organism lives and acts. To Canguilhem (2003, p. 188), Uexküll’s operates an inversion of the relation between milieu and organism, with respect to statements saying that organisms are determined by their environment.

  18. These modes of determination are inspired by the analysis made by Uexkull, Canguilhem, and Lewontin.

  19. My translation of the French: “le propre du vivant, c’est de faire son milieu, de se composer son milieu.”

  20. The “traits” mentioned here probably refer to variations if natural selection can target them.

  21. “Species inheriting nearly the same constitution from a common parent and exposed to similar influences will naturally tend to present analogous variations” (Darwin 1861, p. 152).

  22. Although circumstances and environment are not exactly synonymous, one can grossly consider that they refer, in this context, to the same set of elements.

  23. In this respect, the inherited niche would include any environmental elements, in addition to those that are traditionally mentioned (spider web, bird nests, mammal burrows, etc.). It is important to note that the main point of this article is not to criticize the absence of distinction between mere persisting environment and inherited environment, but rather to criticize the very concept of environmental inheritance. However, this analysis also shows that the criterion of “causal dependance on parents” would not be relevant to distinguish between inherited and non-inherited environments.

  24. For example, while beaver dams could be considered, at a given spatiotemporal scale (e.g., two generations), as part of beavers’ legacy notably because they allow them to channel flows of matter and energy (inheritance), they could, at another scale (fifty generations) be considered as part of beavers' selective environment, notably because they could favor some morphological or physiological traits in the long run.

  25. As mentioned above, I consider that the concept of constructed niche is theoretically equivalent to that of biological environment, given that there is no such thing that could be called a biological environment and that would not be determined, lato sensu, by the organisms that occupy it.

  26. They start with a functional/developmental definition of constructed niche and then indicate that the latter “may influence a population’s selective environment” (p. 118).

  27. Sterelny considers that niche construction only occurs when organisms adapt their local environment (2005, p. 29).

  28. This perspective differs from those that consider that some elements can be at the same time parts of the environment and of extended biological systems (Turner 2000, pp. 6–7; Stotz 2010, p. 492).

  29. Organizational closure is distinct from thermodynamic openness Moreno and Mossio 2015). Biological systems are far from equilibrium thermodynamically open systems, maintained through the continuous flows of matter and energy that traverse them. This flow is channeled by a set of organized and interdependent objects, which are called "organizational constraints” and which are engaged in a circular causality. Constraints are said to realize closure in this precise meaning.

  30. For more details about the categories of objects derived from an organizational framework, see Mossio and Pontarotti (2019).

  31. The trans-generational stability of hatching plants is explained by imprinting mechanisms (Mameli 2004). Presented as an example of inherited environment by Mameli (2004), it is not included in biological legacies in an organizational framework.

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    Gaëlle Pontarotti

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Pontarotti, G. Environmental Inheritance: Conceptual Ambiguities and Theoretical Issues. Biol Theory 17, 36–51 (2022). https://doi.org/10.1007/s13752-020-00348-5

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