Splitting niche construction

I have recently had an interesting e-mail conversation with Tom Meli. We were discussing part of a recent paper by Tom Dickins (TD) and I. The overall thesis TD and I advanced was that recent attempts to construct heterodox evolutionary theories, at odds with the New Synthesis, are failing because natural selection is both necessary and sufficient to explain design. In our view, many forms of heterodox argumentation founder because they tacitly assume that selection is not necessary (see our paper for detail). But the existence of all sorts of complex ecological interactions, which might be expected to create novel evolutionary outcomes, seems to undermine our claim that natural selection is sufficient. Taking an orthodox example, the Red Queen hypothesis shows how host-parasite interactions can provide selection pressures required for the evolution of sex.

The original Red Queen hypothesis is named after the character in Lewis Carroll’s “Through the Looking Glass” who had to run constantly to stay in the same place, and posits a cyclical change between two or more resistance alleles in a population of hosts that is caused by and causes a lagged cycle of cognate virulence alleles in parasites. In a cyclical “arms race” of this sort either participant (hosts or parasites) can benefit by producing varied offspring and sex is one way to achieve this. Modern versions include the idea that, since parents bequeath parasites to offspring, there is an added incentive for producing varied offspring: dissimilarity from the parents abrogates what would otherwise be a head-start for an evolving parasite population in any given offspring (Agrawal, 2006). Now while selection may be necessary in this example it is surely illegitimate to state that it is sufficient. Host-parasite interactions, and perhaps a kind of extra-genetic inheritance, are also required (see our paper for a discussion of the role of non-genetic inheritance).

Tom Meli’s question also relates to our sufficiency claim. He wanted to know why we were critical of the niche constructionist perspective. Crudely niche construction is described as a kind of feedback process in which an organism’s impact on its environment alters conditions in such a way that the selection pressures on the organism change. In common with the Red Queen, this does not shun a necessary role for selection and the claim that niche construction is a “neglected process in evolution” (Odling-Smee et al., 2003) doesn’t in itself amount to the claim that natural selection is unnecessary. No indeed, although, to be fair, TD and I did believe this was implied; but I believe our sufficiency claim is justified and that niche construction falls foul of it.

The reason for this is that we are talking about necessity and sufficiency of selection for design. Here design means the adaptive fit between an organism and its environment. In the Red Queen, the environment is a rapidly (and cyclically) changing one and selection provides a solution: sex. Sex should only be considered a design in respect of those particular selection pressures to which it represents a solution and not outside this context. We are not claiming that selection is necessary and sufficient for any biological feature in any context. Indeed half the explanatory battle is to reveal the sorts of dynamics in response to which one may consider a feature a design.

This argument can be extended by considering the nature of niche construction in more detail. Niche construction is not a kind of selection, but perhaps it is a kind of ecological process. TD and I are sceptical of this. The dynamics captured by niche construction can be split into different kinds. This is also true of the Red Queen, but these dynamics are instrumentally lumped together as those that create an advantage for high genetic variance in offspring (note that the Red Queen is not the only theory and that broader lumping is perhaps more productive: see West et al., 1999). The evolutionary consequences of niche construction seem more varied than this and it is not clear what it causes selection for.

Another comparison is to sex itself. While both sex and niche construction are consequences of selection, they also lead to different kinds of selection, the former being a pre-requisite for sexual selection and the latter, for natural selection. Here is a hierarchy of concepts with sex and niche construction at a higher level and sexual and natural selection at the lower level. Sex is easily defined as the presence of two or more self-incompatible mating types and, among other things, this can lead to a kind of selection that is characterised by a different mechanism from natural selection. Traditionally female choice is the agent of selection in sexual selection and differential survival, in natural selection. Because both kinds of selection entail differential reproductive success they can be lumped together, but they do show differences in mechanism. Although selection resulting from niche construction is different from sexual selection it is not clear how it mechanistically differs from any other kind of natural selection resulting from, say, high temperature or overcrowding.

So niche construction is hard to define in itself (cf. sex), in terms of the kind or mechanism of selection that results (cf. sex) or in terms of what it causes selection for (cf. the Red Queen). This is not to say that the various dynamics lumped together under niche construction do not have consequences for evolutionary outcomes. It is just the lumping we object to, as it doesn’t appear to serve any useful purpose. We believe the fact that a set of difficult to model feedback processes are important in evolution does not justify their elevation to the status of a singular and neglected process.

Postnote: This is an extension of a debate with Tom Meli, so please read the comments to hear his side of the argument…