Journal club of one: ‘Splendor and misery of adaptation, or the importance of neutral null for understanding evolution’

In this paper from a couple of years ago, Eugene Koonin takes on naïve adaptationism, in the style of The Spandrels of Saint Marcos and the Panglossian paradigm (Gould & Lewontin 1979). The spandrels paper is one of those classics that divide people. One of its problems was that it is easy to point out what one shouldn’t do (tell adaptive stories without justification), but harder to say what one should do. But anti-adaptationism has moved forward since the Spandrels, and the current paper has a prescription.

Spandrels contained a list of possible alternatives to adaptation, which I think breaks down into two categories: population genetic alternatives (including neutral or deleterious fixations due to drift and runaway selection driving destructive features rather than fit to the environment), and physiological or physical alternatives (features that arise due to selection on something else, which are the metaphorical spandrels of the title, and fit to the environment that happens due to natural laws unrelated to biological evolution).

Eugene Koonin elaborates on the population genetic part, concentrating more on chance and less on constraint. He brings up examples of molecular structures that may have arisen through neutral evolution. The main idea is that when a feature has fixed, it doesn’t go away so easily, and there can be a ratchet-like process of increasing complexity. Evolution doesn’t Haussmannise, but patches, pieces, and cobbles together what is already there.

As a theoretical example, Michael Lynch (2007) used population genetic models to derive conditions for when molecular networks can extend and become complex by neutral means. (Spoiler: it’s when transcription factor binding motifs arise often in the weakly constrained DNA around genes.) Eugene Koonin thinks that the thing to do with this insight is to use it as a null model:

A simplified and arguably the most realistic approach is to assume a neutral null model and then seek evidence of selection that could falsify it. Null models are standard in physics but apparently not in biology. However, if biology is to evolve into a ”hard” science, with a solid theoretical core, it must be based on null models, no other path is known.

I disagree with this for two reasons. I’m not at all convinced that biology must be based on setting up null models and rejecting them … or that physics is. In some statistical approaches, inference proceeds by setting up a null hypothesis (and model), and trying to shoot it down. But those hypotheses are different from substantial scientific hypotheses. I would suspect that biology spends too much time rejecting nulls, not too little.

Bausman & Halina (2018) summarise the argument against null hypotheses like this in their recent paper Biology & Philosophy:

The pseudo-null strategy is an attempt to move hypotheses away from parity by shifting the burden of disproving the null to the alternative hypotheses on the authority of statistics. As we have argued, there is no clear justification for this strategy, however, so the hypotheses should be treated on a par.

That is, they reject the analogy between statistical testing and scientific reasoning. They take their examples from ecology and psychology, but there is the same tendency in molecular evolution.

Also, constructive neutral evolution is as a pretty elaborate process. Just like adaptation should not be assumed as a default model without positive supporting evidence, neither should it. The default alternative for some elaborate feature of an organism need not be ‘constructive neutral evolution’, but ‘we don’t know how it came about’.

On the other hand, maybe the paper shouldn’t be read as an attempt to set constructive neutral evolution up as the default, but, like Spandrels, to repeat that adaptation isn’t everything:

It is important to realize that this changed paradigm by no means denies the importance of adaptation, only requires that it is not taken for granted. As discussed above, adaptation is common even in the weak selection regime where non-adaptive processes dominate. But the adaptive processes change their character as manifested in the switch from local to global evolutionary solutions, CNE, and pervasive (broadly understood) exaptation.

Naïve adaptationism is certainly not dead, but just whisper \frac {1}{N_e s} and the ghost goes away. I would have been more interested in an attack on sophisticated adaptationism. How about the organismal level? Do ratchet-like neutral processes bias or direct the evolution of form and behaviour of say animals and plants?


Bausman W & Halina M (2018) Not null enough: pseudo-null hypotheses in community ecology and comparative psychology Philosophy & Biology

Gould SJ & Lewontin R (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme Proceedings of the Royal Society B.

Koonin EV (2016) Splendor and misery of adaptation, or the importance of neutral null for understanding evolution BMC Biology.

Lynch M (2007) The evolution of genetic networks by non-adaptive processes Nature Reviews Genetics.