The generality of Constructive Neutral Evolution

Abstract

Constructive Neutral Evolution (CNE) is an evolutionary mechanism that can explain much molecular inter-dependence and organismal complexity without assuming positive selection favoring such dependency or complexity, either directly or as a byproduct of adaptation. It differs from but complements other non-selective explanations for complexity, such as genetic drift and the Zero Force Evolutionary Law, by being ratchet-like in character. With CNE, purifying selection maintains dependencies or complexities that were neutrally evolved. Preliminary treatments use it to explain specific genetic and molecular structures or processes, such as retained gene duplications, the spliceosome, and RNA editing. Here we aim to expand the scope of such explanation beyond the molecular level, integrating CNE with Multi-Level Selection theory, and arguing that several popular higher-level selection scenarios are in fact instances of CNE. Suitably contextualized, CNE occurs at any level in the biological hierarchy at which natural selection as normally construed occurs. As examples, we focus on modularity in protein–protein interaction networks or “interactomes,” the origin of eukaryotic cells and the evolution of co-dependence in microbial communities—a variant of the “Black Queen Hypothesis” which we call the “Gray Queen Hypothesis”.

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Notes

  1. 1.

    Complexity is of course an onerous notion, highly dependent on context. Increases or decreases in its value might nevertheless be assessed—in terms of the interdependency of component parts or some product of the number of parts compared to part-types—with less ambiguity than assigning definite values to particular entities.

  2. 2.

    Indeed, Koonin (2016) describes subfunctionalization as the clearest cases of the “evolutionary modality” of CNE.

  3. 3.

    Gene duplication is also, of course, a source of “new genes” as when one duplicate acquires a novel function (“neofunctionalization”; Lynch and Conery 2000; Lynch and Force 2000) or when each of the duplicate pairs retains a subset of the functions of a their multi-functional common ancestor. Such “subfunctionalization” (Lynch and Conery 2000) comprises CNE as we define it below (pre-suppression followed by ratcheting).

  4. 4.

    In the case of bacterial cells, Golding and Cox (2006) report that on time scales longer than a second, “the motion of the RNA molecule is dominated by interactions with obstacles in the medium surrounding it”—interactions we expect only to be amplified in more complexly compartmentalized eukaryotes.

  5. 5.

    That such proteins are functional can be verified biochemically or by amino acid sequence similarity to homologous proteins in closely related organisms that do not have RNA editing.

  6. 6.

    The Black Queen gets its name from the game of Hearts, where the goal of the game is to avoid being stuck with the queen of spades; likewise the goal is to avoid being stuck with certain costly genes. We term the CNE variant of the BQH the Gray Queen Hypothesis, to emphasize the likeness of both views, the absence of an all-or-nothing approach to selection, and since gray is a neutral colour.

  7. 7.

    Something important is neglected thereby, and accepting CNE as a co-equal force to selection might help us recognize this level. It is after all this level that is the focal point of contemporary “systems biology” (Ideker et al. 2001).

  8. 8.

    One could also cite so-called “moonlighting proteins”. These have well-known and likely more ancient functions, but have been “recruited” to serve additional important roles in basic transcriptional or translational processes (or as crystallins in the vertebrate eye and as tumor suppressors). Presumably these associations (even if subsequently “improved by positive selection”) began as fortuitous interactions with pre-existing cellular entities (Jeffery 2003).

  9. 9.

    Moreover, as discussed in the next section, it may be a multi-species microbial community rather than a single prokaryotic cell that is appropriately compared to a eukaryotic cell.

Abbreviations

CNE:

Constructive Neutral Evolution

PPI:

Protein–protein interaction networks

ZFEL:

Zero-force evolutionary law

BQH:

Black Queen Hypothesis

GQH:

Gray Queen Hypothesis

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Acknowledgements

We thank Dr. S. A. Inkpen, and the Dalhousie-Kings STS reading group for helpful comments, and NSERC Discovery Grant GLDSU 447989 for support.

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Brunet, T.D.P., Doolittle, W.F. The generality of Constructive Neutral Evolution. Biol Philos 33, 2 (2018). https://doi.org/10.1007/s10539-018-9614-6

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Keywords

  • Constructive Neutral Evolution
  • Evolution of complexity
  • Black Queen Hypothesis
  • Eukaryogenesis
  • Protein–protein interaction networks
  • Interactome