Clatterbuck et al. (Biol Philos 28: 577–592, 2013) argue that there is no fact of the matter whether selection dominates drift or vice versa in any particular case of evolution. Their reasons are not empirically based; rather, they are purely conceptual. We show that their conceptual presuppositions are unmotivated, unnecessary and overly complex. We also show that their conclusion runs contrary to current biological practice. The solution is to recognize that evolution involves a probabilistic sampling process, and that drift is a deviation from probabilistic expectation. We conclude that conceptually, there are no problems with distinguishing drift from selection, and empirically—as modern science illustrates—when drift does occur, there is a quantifiable fact of the matter to be discovered.
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Brandon and Nijhout (2006) discuss and visually represent this gray zone in a treatment of the conditions under which we expect selection to dominate drift and vice versa. See especially Fig. 2, p. 285.
Chance set-ups are, in our view, causal set-ups. We are unsure of whether Clatterbuck et al. mean something else by this term.
One reason one might think that there is a difference in the processes of drift and selection is that the demographic facts that determine N operate on the entire genome while the ecological facts that determine s at a particular genetic locus operate (to a first approximation at least) locally. However, if it is Ns that is the critical parameter for drift, it acts locally just like s. That is, the genome-wide effect of N is filtered through the selective forces acting at a particular locus to produce the value of Ns that applies at that locus.
There are also some non-comparative methods. For example, Wallace et al. (2013) estimate the strength of selection on codon usage based on experimental data and the genome sequence in Saccharomyces cerevisiae. Another (somewhat controversial) example is based on codon “volatility” and applicable to a single genome (see Plotkin et al. 2004).
The main difficulties have to do with linkage. For instance, if substitutions in the third position of a codon are synonymous (and so, to a first approximation, neutral) while mutations in the first two positions are not, this sets up the comparison at the heart of the MK method. However, obviously the fate of the third position is not independent of the first two. If directional selection is acting, then the nucleotide that happens to be in the third position is tugged along with the selected nucleotide combination at positions one and two. This is called hitchhiking. But what this means is that when directional selection is acting, the third position is not in fact acting in a way that instantiates the proper null model.
The “alternative” to directional selection is not drift. There are multiple alternatives in addition to drift, most importantly, stabilizing selection.
Note that hitchhiking is not a problem for this comparison.
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We wish to thank the philosophy of biology reading group at Duke University and an anonymous reviewer for helpful comments. Special thanks go to David McCandlish for help with some final tweaks.
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Brandon, R., Fleming, L. Drift sometimes dominates selection, and vice versa: a reply to Clatterbuck, Sober and Lewontin. Biol Philos 29, 577–585 (2014). https://doi.org/10.1007/s10539-014-9437-z
- Probabilistic sampling
- Causal relevance