Natural selection is the most important process in evolution.
The meaning of this statement depends on how importance is judged and on what is meant by evolution. So, for precision, what I will actually defend in this posting is the proposition that natural selection is always necessary, if not sufficient, to explain adaptive evolution, by which I mean change between generations which improves the fit between an organism and its environment.
This statement is general because it applies to as yet unexamined cases. So it might seem to be an anti-empirical claim. It is not meant that way; data should be collected and hypotheses tested (as it already has been in support of evolution by natural selection in particular instances). It is just that whatever is revealed about the evolutionary processes leading to adaptation in any particular case will, I believe, always evidence or logically invoke natural selection in a non-trivial role. I would like to contrast this “strong” position with a “weak” one that says that natural selection cannot be credited with an essential role until this evidence is collected. It needs stressing at this point that evolution (in the sense of descent with modification) is massively evidenced across the board (biogeography, fossil record, vestigiality, sequence data, genetic codes, experimental evolution, etc.) and that’s not what’s at issue here.
What kind of objections can there be to this? Obviously creationists (also read “intelligent design theorists”) will not agree with me – mostly, of course, because they are committed to and trying to justify a particular theistic worldview that is plausible only if one is ignorant of the facts supporting evolution in general. Such pretend rationalism is so much fluff and anyone interested needs to learn a lot of relevant facts and should buy a decent textbook on evolution rather than reading blogs (try this). But, as we shall see, my specific proposition might seem to be at odds with some scholarly opinion.
It is likely that natural selection plays a trivial role in the evolution of eukaryotic genome structure. This is the core argument of a recent paper by Michael Lynch published in the Proceedings of the National Academy of Sciences USA. (Note that Lynch has written this paper also and a book reviewed here). Long-understood, but often-overlooked non-selective processes better account for the emergence of higher level properties such as (genetic) complexity, modularity (in development) and evolvability (the ability to respond to selection and generate novelty). Lynch’s polemical point is that there are only four major evolutionary “forces”: mutation, recombination, genetic drift and natural selection, and that the field of population genetics already provides all the mathematical tools needed to analyse the relative significance of these. (Nothing is said about migration’s impact). Paying particular attention to genetic drift he emphasises that these tools should be regularly used to test non-adaptive explanations.
Genetic drift is akin to sampling error in statistics. It tends to occur in small populations of organisms when each generation is constituted from a small sample of the gametes produced. The average proportions (or “frequencies”) of gene copies (or “alleles”) in small samples tend to deviate by chance from those in the population from which they are sampled. In this way a new mutant allele can be lost from a population or can increase in frequency so that all individuals carry it. Genetic drift can be strong enough to scupper natural selection if the fitness benefit of a new allele is small and therefore not instantiated in differential reproductive output. The key point for Lynch is that the population size (or more technically the effective population size) is small in multicellular eukaryotes and this permits the accumulation of genetic novelties such as introns (non-coding segments located within gene-coding regions) with mildly deleterious phenotypic consequences (considered individually). From this perspective Lynch takes a swipe at Dawkins whose “agenda to spread the word on the awesome power of natural selection”, at the expense of other evolutionary mechanisms, represents “a view that is in some ways profoundly misleading”.
Now being a theoretical pluralist, having an open mind about the relative role of all evolutionary processes as Lynch proposes, sounds like a good idea. But my point is that, where adaptive evolution is concerned, we can expect a role for natural selection. This suggests that, taking into account his didactic role, we may at least partially forgive Dawkins. The existence of adaptation is striking and invites public curiosity. Unfortunately it also triggers the intuition that a system is designed. So there is an emotional reward in understanding how adaptation works and sometimes work to be done to overcome biases in intuition with the relevant facts. It is no use telling people that most evolutionary change is not adaptive. That is even though it may be true.
Now to defend my main point that natural selection is important for adaptive evolution. Lynch correctly points out that “the effects of mutation and recombination are nonrandom” and that “by magnifying the role of chance, genetic drift indirectly imposes directionality on evolution by encouraging the fixation of mildly deleterious mutations and discouraging the promotion of beneficial mutations.” This is true and makes talk about selection for increased complexity loose talk, but these non-adaptive forces are either random with respect to organismal fitness or detrimental to it. So any explanation of improved fitness and of adaptation to the environment will rely on a process that can discriminate in favour of fitter variants (see my posting on Lamarck below) and this is natural selection. The truth of the weak and strong versions of my position, i.e. whether or not we can always expect natural selection to underlie adaptation, depends on our setting a threshold for the improbability associated with adaptive change in general. If adaptation is unlikely to occur by chance then we can conclude a priori that natural selection is likely. Let me stress again that it is always worth doing the experiments to show it. In particular experimental evolutionary work is useful because it breaks down the process of adaptation by probabilistic steps (and shows why it is not a mere tautology).
Now the main problem with my position so far is that it is not always easy to know whether or not something is an adaptation, let alone assess it’s improbability under non-selective scenarios as Lynch does. Probably the best-known criticism of adaptationism was made in Gould and Lewontin’s 1979 famous spandrels paper. Some of the literary allusions in this piece have taken on a life of their own since and it common to hear criticisms of adaptive hypotheses to the effect that they are “just-so stories”. Perhaps less common is the assertion that the adaptationist programme is a result of a “Panglossian” imagination. This is one that sees all phenomena as explained by their current function, i.e. one in which adaptation is presumed to be omnipresent. (This is like Dr. Pangloss, a character in Voltaire’s Candide, who thought that everything in this world was for the best and who constructed tenuous explanations to fit his supposition – a lampooning of theology).
When these criticisms are merely asserted they are, in my view, patently unfair. Many adaptive stories are subjected to testing (Lynch is adding value here) and the attractiveness of adaptive explanations cannot be taken to automatically disqualify them. To be fair to Gould and Lewontin, they did not just make these assertions. Instead they suggested “a partial typology of alternatives to the adaptationist programme”. Genetic drift as a source of non-adaptive evolutionary change was discussed although the paper’s thrust was morphological evolution. Lynch seems to be expanding on this for the molecular age by marrying molecular biology and population genetics. The take-home point is that these tools can be more widely applied to tighten up the science.
So far so good, but where does Lynch’s thesis take people who are thinking seriously about evolution and behaviour? Will it always be impossible to find support for natural selection on complex behavioural traits without first identifying the responsible genes and then analysing them using appropriate algorithms or at least gathering relevant population data? Can we make any general statements about the relative role of natural selection on traits “higher up” the phenotypic scale?
Well I reckon there are good reasons to think that most change at the genetic level is due to drift (chief among these is small population size in multicellular organisms as noted by Lynch) and as described there are good reasons to think that most adaptive behavioural and morphological change is due to selection. This seems like an interesting paradox: that as we move “up” the phenotypic scale the prior probability of natural selection increases, although of course it is perfectly reasonable to suppose that most visible changes are underlain by only a subset of changes at the genetic level. An alternative interpretation is that traditional biologists and evolutionary psychologists tend to find interesting things adaptive (the Panglossian tendency). I submit, instead, that they find adaptive things interesting and tend to ignore non-adaptive things like having precisely five fingers. The difference between scientists working at different levels of the phenotypic scale is then simply one of what interests them rather than something fundamental about evolution at different levels or which side of some great theoretical schism they fall.
I also think that arguments about complexity, modularity and evolvability are distractions. I agree with Lynch on these in that I think the prior probability of selection is low for these too (and perhaps we can fault Dawkins here). (Any thoughts on modularity of mind here – or is this too tenuous a link?)
So to sum up – the only a priori plausible mechanism for adaptive change is natural selection (possibly there are self-organising properties at lower probabilities) and discussions about how significant it is should take this into account the centrality of adaptation in the field under review. As good scientists though we should seek independent evidence for natural selection and try to exclude more chancy processes. And we should be wary of labeling something adaptive when it is not. Looking for evolution by natural selection we are thus between Scylla and Charybdis. They can each swallow a lot of sea water – but nobody need doubt the existence of a channel through or feel any compunction in charting this voyage for public edification and enjoyment.