Although most mutations in the DNA that affect fitness are harmful, without mutations there would be no evolution. Evolution depends on the genetic variation created by mutation, and although there are other ways to change DNA beyond conventional mutations (horizontal gene transfer is one, though in effect it acts like a big mutation), in general evolution would pretty much come to a standstill without those random errors in the DNA. That a small fraction of the random errors increase the propagation of their gene copies (usually by improving the reproductive output of individuals carrying those good mutations) is why we have all the species and adaptations on Earth today.

The irony to which I refer in the title is that natural selection would in principle—and has in practice—actually tried to reduce the frequency of mutations to zero. But if this process were perfectly successful, natural selection would put itself out of business by totally eliminating the creation of genetic variation. We know that selection has “tried” to do this, for all the intricate mechanisms for repairing DNA damage, and excising new mutations, are products of natural selection. Those mechanisms operate not only in the “somatic” cells of the body, but also in the cells that ultimately produce sperm and eggs.

So natural selection acts on the DNA-repair level to put itself out of business. Why hasn’t it? Why are organisms still evolving? I see only four answers, one more likely than the other three.

The most probable explanation is that evolution does not produce perfect adaptations. In the case of mutations, though natural selection favors individuals most able to repair any changes in DNA (although a small percentage of these might be adaptive), this level of perfection cannot be achieved because of constraints: the cost of achieving perfection, the fact that all errors are impossible to detect or remove, or that some cells (i.e., sperm or eggs) may not even have DNA-repair mechanisms because of genetic or physiological constraints.

A less likely explanation is that the imperfection of DNA-repair mechanisms is itself an adaptation. That is, selection has acted to favor imperfect repair because such perfect repair would lead to organisms that are maladapted when the environment changes and new mutations are required to adapt. I don’t see this as likely because most mutations would still be deleterious (DNA-repair processes have no way to distinguish between useful and harmful mutations), and because this kind of selection would require frequent changes of the environment.

The third mechanism, conceptually related to the second, is that selection could favor a reduced level of DNA repair, or a higher rate of mutations, when the organism senses that the environment is changing. We know that stressed bacteria have a higher mutation rate, but that doesn’t seem to be a result of natural selection; it’s likely an epiphenomenon of stressful conditions like heat or a change in the chemistry of the substrate. But we can show theoretically that if the environment changes often enough, natural selection could favor a general increase in mutation rate because the generation of lots of bad mutations is more than counterbalanced by the few good mutations needed to survive. This is called selection for “adaptability” or “evolvability.” But there’s little evidence that a general increase in mutations under stress or changed environments is either a general phenomenon or, when present (as in bacteria) has resulted from natural selection.

Finally, there is a group-selectionist explanation. This posits that some species have indeed managed, via natural selection, to achieve near perfection in eliminating mutations, but those species went extinct because they couldn’t respond to environmental change. That would leave us with only those species having imperfect mechanisms for detecting and repairing mutations—what we see today.

I see this form of group selection as improbable, because although group selection would oppose a reduction of mutation rates toward zero, individual selection would oppose that trend. Thus, selection for imperfect DNA repair would require that the rate of group extinction or differential reproduction outpaces outweigh the rate of different reproduction of individuals that favors ever-reduced mutation rates. When group and individual selection act in different directions, as they do for traits like altruism, it requires a substantial rate of group extinction or group propagation to fix a trait; and even when if imperfect repair became the group norm, natural selection on individuals would again start driving mutation rates toward zero.

In the end, the irony of natural selection is that it tends to put itself out of business. But it hasn’t been able to, because, in my view, natural selection can’t create absolute perfection. In the case of mutations, selection isn’t able to completely weed out new errors in the DNA.

I may be wrong in these musings, or may have missed some explanations, but I’m largely unable to brain today and so am just offering this for your consideration.