Abstract
This paper investigates the complexity hypothesis in microbial evolutionary genetics from a philosophical vantage. This hypothesis, in its current version, states that genes with high connectivity (more functional connections to other genes) are likely to be resistant to being horizontally transferred. We defend four claims. (1) There is an important distinction between two different ways in which a gene family can persist: vertically and horizontally. There is a trade-off between these two modes of persistence, such that a gene better at achieving one will be worse at achieving the other. (2) At least some genes are likely to experience selection favoring increased transferability. One consequence of this can be encapsulated as the “simplicity hypothesis”: horizontally persisting genes will experience selection favoring reduced connectivity. (3) In order to make sense of the simplicity hypothesis, we need to consider evolutionary populations that transcend species boundaries. Vertical and horizontal persistence are therefore not two competing ways of succeeding at the same game, but involve playing two different games altogether. (4) The complexity hypothesis can be understood in terms of two related notions: entrenchment and Cuvierian functionalism. This framing reveals previously unrecognized and philosophically interesting connections between reasoning about deep conservation and horizontal transfer.
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Notes
We speak of gene family acquisition to distinguish this form of transfer from paralog addition, which also involves gene acquisition.
We raise this point because it constitutes a possible exception to the general existence of an inverse correlation between connectivity and transferability. An anonymous reviewer, however, suggests that this case might not be an exception: low but non-zero levels of coevolution could result in complex poisoning (the transferred protein interacts with the host complex, but dysfunctionally), and thus could render HGT deleterious. In the absence of empirical work, it is difficult to know how to balance these competing reasons.
In making this claim, we are considering only the effects of selection for transferability; other causes (as discussed in the “Vertical and Horizontal Persistence” section) might counteract these effects in real populations.
We are not positing selective processes that favor increased connectivity directly; it is enough for entrenchment to be a byproduct of selective processes. In Sober’s (1984) terms, what is required is selection of increased connectivity, not selection for it.
A quick note on terminology: throughout this section we will exclusively use “step” to refer to particular moves in the Cuvierian argument pattern, and “stage” to refer to temporal parts of organismal and evolutionary processes (e.g., developmental stages, stages of successful HGT).
Because of these features, Cuvierian functionalism can seem to suggest that species have fixed “types”, ignoring the variability of real populations. However, Cuvierian functionalism ultimately rests on a kind of selective process (filtering out of variants that disrupt integration), and thus requires variability. An explanation of stasis in terms of the absence of variants would not be Cuvierian functionalist. See Novick (2019) for a full discussion of these issues.
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Acknowledgments
The authors would like to thank Bill Wimsatt, Joe Bielawski, Fabien Denis-Cayer, Maureen O’Malley, and two anonymous referees for Biology and Philosophy for comments on the manuscript, as well as Jeremy Wideman and Chris Jones for helpful discussion. This work was supported by the Natural Sciences and Engineering Research Council of Canada, Grant Number GLDSU/447989.
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Novick, A., Doolittle, W.F. Horizontal persistence and the complexity hypothesis. Biol Philos 35, 2 (2020). https://doi.org/10.1007/s10539-019-9727-6
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DOI: https://doi.org/10.1007/s10539-019-9727-6