Robustness: a new battlefield in the evolution wars?

This is another archival repost from the old blog, originally written in oct 2007.

Evolution, from the point of view of the geneticist, is the change in allele frequencies that occurs in populations over time. New alleles are created by random mutation, and others slowly disappear through natural selection or pure chance (“genetic drift”). When making random changes to a complex and finely tuned system, there are far more ways to break it than to improve it. But in fact, the vast majority of mutations have no apparent effect on fitness at all. There are many layers of redundancy in biology: changing the letters of genes does not always alter the building blocks of the proteins they encode; changing the building blocks of proteins more often than not has little or no effect on the parts of the protein that matter; many genes have more than one copy in the genome; and so on. Much of this has been known since the early twentieth century, and is part of what is called “neutral evolution”.

A similar, but not identical concept is “robustness”. Robustness is essentially a measure of how much change a system can tolerate without loosing its function. Robustness is related to neutral evolution: in more robust systems, a larger proportion of mutations could be described as neutral. Robustness is particularly used for describing networks of components, such as networks of genes activated during development, or signalling networks. Loss or change of function of an individual signalling component is often tolerated because there are several other routes by which the message is transmitted, and so the end result may be unaltered. Robustness would appear to be advantageous: the mutation rate can remain at a level that generates beneficial mutations, and mutations that may prove useful in future situations, without too many deleterious mutations arising; mutations in the somatic cell line do not instantly render a cell useless (though one can imagine this being a bad thing, e.g. in cancer); populations are more varied, which may be beneficial during hard times and environmental change; and so on. So the big questions are: is robustness itself an adaptation (and if so, for the obvious reason, or for a completely different reason?), an accident that has since become advantageous, or just one of many equally good ways that life could work? Is robustness an inevitable consequence of the evolutionary process, either as a product of natural selection or random drift, or both? Is robustness a prerequisite for complex multi-cellular life as we know it? And to what extent do the answers to these questions apply also to the other examples of redundancy described above?

There are a lot of assumptions made about what the answers to these questions are, and they reflect a bigger argument in evolutionary biology. In both the specific and the general arguments, the difference in terminology tends to be bigger than the difference in theory: both sides accept each other’s arguments, they just believe their own to be more important or interesting, and therefore talk about evolution in different terms. The emphasis of the “adaptationist” (pejoratively “Darwinian fundamentalist” and “Panglossian”) camp is on structures created by natural selection; the caricature is that everything in biology has a selective advantage. The emphasis of the opposing (“neutralist” or self-styled “pluralist”) camp is on the role of processes other than selection, i.e. chance, in the form of genetic drift and random long-term trends. In reality, the adaptationists admit a role for non-selection processes, and the pluralists admit the power of natural selection as the explanatory force in biology. The principle difference between the two camps is that, in the absence of evidence either way,adaptationists presume a feature is an adaptation, while neutralists presume it isn’t (and chide the adaptationists for making presumptions). A symptom of this divide is that the pluralists will speak in terms of neutral evolution, and the adaptationists will speak in terms of robustness; neither will admit that both ways of approaching the subject might be useful.

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