The Original Red Queen’s Hypothesis

Leigh Van Valen (who died last month) is well known for being an original thinker. It is perhaps not surprising, then, that the only way he could publish his most famous idea was to start a journal to print it in. Because of this, the paper is devilishly hard to get hold of: I managed to get a photocopy, with only one page of references missing.
This idea dates back to 1973, and is now called the “Red Queen hypothesis”: that fitness is constant over time because of continual changes in the environment. Although this is the way the hypothesis is stated, it is a subtle mis-representation of the original idea. This is because it has been morphed into something a bit different, when the idea was ripped from its palaeontological roots into the world of population and evolutionary genetics.

So what, you are asking, is the paper actually about?
Van Valen takes a palaeontologist’s view of fitness: it’s about extinction. He starts by presenting his data: 6½ pages of survivorship curves (log(number of taxa) against age) for a wide range of taxa. The pages are like this.
Only 2 of 7 figures
The purpose of all of these plots is to demonstrate that the survivorship curves tend to be straight lines, which then suggests that the extinction rate within a taxon is (roughly) constant. He finds a couple of exceptions to this (e.g. due to mass extinction events), but generally the pattern seems to hold. This is surprising: if nothing else, one might expect a concave relationship as younger taxa will cover a smaller area, and this generally implies a higher extinction rate.
On the basis of these data, Van Valen introduces his evolutionary law:

The effective environment of the members of any homogeneous group of organisms deteriorates at a stochastic constant rate.

This of itself would lead to a constant rate of extinction, but it goes beyond the observations by saying that the reason for this is extrinsic: it is the environment that causes extinctions, not anything intrinsic about the taxon.
Although Van Valen found that extinction rates are constant within taxa, he also showed that they vary across taxa. For example, the data show that early trilobites have about double the extinction rate of late trilobites, and even these die off at half the rates of mesozoic ammonites. This leaves Van Valen with a problem:

The probability of extinction of a taxon is then effectively independent of its age. This suggests a randomly acting process. But the probability is strongly related to adaptive zones [roughly, the ecological niche]. This shows that a randomly acting process cannot be operating uniformly. How can it be that extinction occurs randomly with respect to age but nonrandomly with respect to ecology?

He answers this with a (partially verbal) model. Imagine species in the same adaptive zone. If one species becomes more successful, then one can imagine that the others will be negatively impacted. The data suggest that, on average, this is a zero sum game: although at any one time one species may be doing better than another, overall they approximately cancel each other out.
Simplistically, this would lead to a concave survivorship curve, with older lineages having lower extinction rates. The reason for this is simply that the species that do worse – that is, the species with a lower fitness – will go extinct, thus increasing the average fitness. But what’s wrong with this is that it leaves out changing environment. Van Valen’s image of the environment is one which buffets the species with “irregular biotic perturbations”. Most will probably, like earthquakes, be minor with only rare events leading to large extinctions.

[T]he effects of these minor perturbations are not independent of each other over time. If they were, they should not be distributed about a constant mean. The rate of deterioration of the effective environment has what we can descriptively call the property of homeostasis. A large change in one interval is compensated for by a small one later, on the average, and vice versa; the mean itself does not undergo a random walk. It is the organisms in the adaptive zone that can link the perturbations across time in that the effects of one perturbation may depend on the effects of those before it. Species can easily be removed by one kind of perturbation are not there if it comes again soon, and may accumulate if it does not come for a long time. Meanwhile other kinds of perturbations are taking their own toll, more or less independently of the first kind.

The implication here is that the perturbations have to be of different kinds: if it was only one kind, then the species that react negatively to it will continue to do so, and will become extinct, leaving the more successful species.
Van Valen then gets to the heart of how The Red Queen is often perceived:

The Red Queen does not need changes in the physical environment, although she can accommodate them. Biotic forces provide the basis for a self-driving (at this level) perpetual motion of the effective environment and so of the evolution of the species affected by it.

Our perturbations can be due to species (e.g. pathogens or predators) changing (for example as they evolve). Within an ecosystem, there will be many species interacting with those in the adaptive zone we are considering. I am not about the relative importance of biotic and abiotic effects: it strikes me as a difficult question to answer in practice, as one would need to account for many species.
Van Valen also raises a couple of other points: first that the Red Queen might explain apparently constant rates of evolution just as well as neutral models: this is important because it suggests we may not be able to estimate truly neutral dynamics without a lot more data. Secondly, the Red Queen does not deny progress: she is happy for species to improve over time, but they are still being buffeted by different forces. And lineages can also increase in size through diversification: she is not concerned with speciation.
At the end of his paper, Van Valen has a short reflection:

From this overlook we see dynamic equilibria on an immense scale, determining much of the course of evolution by their self-perpetuating fluctuations. This is a novel way of looking at the world, one with which I am not yet comfortable. But I have not yet found evidence against it, and it does make visible new paths and it may even approach reality.

I don’t know about Leigh Van Valen, but think that over time evolutionary biology has become more at ease with this dynamic point of view. It is one which sits easily in how I view the real world. There are also fascinating echoes of these ideas in ecology: the neutral theory of biogeography also makes similar zero-sum assumptions (but then, disastrously in my opinion, leave out perturbations from the environment).
The notion of perturbations creating a constant shift in fitness was taken up by evolutionary geneticists, and used in explanations for why sex evolved; something a bit different. This is a reminder of how important broad ideas are. It’s not the details of his paper that became important, or even the original conception of the Red Queen. Both of them have (largely) been forgotten or superseded. But the vision of how populations evolve dynamically in an environment that is constantly throwing all sorts of slings and arrows at communities is what has survived. It is sad that we now see that the idea has outlasted the man, but hopefully it will outlast him for many more years.

Citation

Van Valen, L. (1973). A new evolutionary law Evolutionary Theory, 1, 1-30