Thursday, February 12, 2009

Darwin's 200th: Red Queen And The Lives Of Species

Do species behave like individuals? Do they show the effects of aging reflected in an increased probability of extinction with age?

Darwin argued that natural selection acted at the level of the individual and consequently one type of individual was favored over another. According to him it was competition between individuals within a species that was the engine of evolutionary change.

“But the struggle almost invariably will be most severe between the individuals of the same species, for they frequent the same districts, require the same food, and are exposed to the same dangers.”

But he also recognized the possibility of competition between species leading potentially to species selection.

"The affinities of all the beings of the same class have sometimes been represented by a great tree. I believe this simile largely speaks the truth. The green and budding twigs may represent existing species; and those produced during each former year may represent the long succession of extinct species. At each period of growth all the growing twigs have tried to branch out on all sides, and to overtop and kill the surrounding twigs and branches, in the same manner as species and groups of species have tried to overmaster other species in the great battle for life."

Species selection is analogous to natural selection acting between individuals. With species selection an evolutionary pattern develops as one type of species is favored or another. For example long lived species may give rise to more descendant species than short lived species. Longevity is a species level property, controlled by say a large versus small geographic range. Over time long lived species may become more numerous than short lived species. So, certain types of species proliferate if they have higher rates of speciation or lower rates of extinction. Darwin didn't really develop this concept. The fossil record in his days was poor and there was no way to test any theory of species selection.

I love palaeontology. I am not much of a fossil collector but I like to understand evolution through fossils. I had two paleontologists on my Ph.D committee. My major adviser who also knew a lot about carbonates and another guy who worked almost exclusively on evolution. This post is based on their work on evolutionary patterns in Mesozoic and Cenozoic planktonic foraminifera.

In the early 1970's University of Chicago paleontologist Leigh Van Valen applied survivorship analyses to fossil taxa. This type of analysis is usually done to understand mortality patterns in a population. So in a sample what fraction of individuals died at childbirth, how many as small children, how many as teenagers, and so on at successive intervals. The results are survivorship curves like the one below.

So depending upon socio-economic conditions, parasite loads and other controls a population may be categorized as type I, II or III. Type I is in which mortality rates of the elderly are high. Type III is one where juvenile mortality is high. And Type II is one where the probability of dying is not age depended. The odds of dying at any age are about the same.

Now you would intuitively expect species to show a type III sort of a curve. A newly formed species may not have developed adaptations to a changing environment. But as time goes by the fit between the individuals and the environment increases and so the probability of a longer lived species going extinct decreases. Instead Van Valen found that extinction patterns in fossil taxa follow curve II. The probability of extinction of species is age independent. This became know as Van Valen's law of constant extinction.

Remember to avoid this misunderstanding. The rate of extinction is not constant.


During major environmental perturbations, for example after a meteorite strike, the rate of extinction will increase precipitously. What Van Valen found was that the probability of extinction does not depend of how young or well established (old) the species is. Species of any age have the same chance of going extinct.

Enter the Red Queen. In Lewis Carroll's fantasia novel Through the Looking Glass the Red Queen says to Alice:

`Now, HERE, you see, it takes all the running YOU can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!’

Using this wonderfully quirky analogy Van Valen argued that species too are running faster and faster but stay in the same place relative to other species. This happens because species interact with other species in its environment. If a gazelle evolves a slightly faster speed of running so will its predator the cheetah. If a parasite evolved a new dodge to its host immune system, the host will evolve a new way of stopping the parasite. Species may change in an absolute sense but they remain the same relative to their competitors.

And so the extinction probability is stochastically constant with respect to species age.

My advisers along with their students have been testing the Red Queen prediction in a long drawn out study using Mesozoic and Cenozoic planktonic foraminifera. Their recent results have been published in the journal Palaios. Plantonic foraminifera are particularly well suited for survivorship analysis since they have a really good fossil record and their ranges are well known.

After crunching the numbers the results showed that extinction is usually random with respect to age except during major extinction events. There is a significant deviation from Red Queen behavior at and after the Cenomanian-Turonian extinction event and after the late Cretaceous-Tertiary extinction event (the one that did in the dinosaurs). This pattern is seen in figure below ( beta coeff. of zero is ideal Red Queen behavior) where the upward spikes around 96 mya ( C-T event) and 65 mya (K-T event) represent deviation from the Red Queen prediction of constant extinction probability.

Now the pattern of deviation was peculiar in that it showed that the extinction probability increased with species age . It resembled the Type 1 survivorship curve I put up above. Just like individuals, species seem to be going through senescence.

That doesn't make sense. Species don't senescence. An individual exists between the time of birth and the time of death. A species too exists between times of its origin and extinction. But at any one time of its historical range a species is made up of populations of individuals who age and die and are replaced by the next generation of individuals, an unbroken ancestor descendant series.

Yet planktonic foraminifera species after mass extinctions were behaving like individuals, going extinct as they grew older.

The most likely explanation is that during mass extinctions certain types of species were more likely to adapt and survive and the subsequent evolutionary pattern of these survivors was showing up as age dependence of extinction. Postmassextinction species tend to be made up of small sized individuals. Small size is an indicator of early sexual maturity. So these species are characterized by adults who reach sexual maturity early in life and stop growing.

These types of species are rapid evolving taxa. This is because individuals have short generation time. The rate of evolution depends on generation time and not absolute time (bacteria evolve quicker than elephants). During times of environmental disturbances it is these rapid evolvers that can keep adapting to the changing environment and make it through. Using the Red Queen metaphor, if species keep running to stay atop a moving adaptive peak, during times of crises only the sprinters among them keep pace with the rapidly changing conditions.

If you want to get somewhere else, you must run at least twice as fast as that!

As conditions improve after the mass extinction the survivor species retain their rapid response characteristic and keep evolving quickly and eventually get transformed into new morphospecies. It appears that they have gone extinct. So the pattern of increase probability of extinction with species age results from populations of post extinction species evolving rapidly into new species, a process known as pseudoextinction.

How do we understand this in terms of selection acting at different levels of biological organization?

Here again selection is acting on two levels. During environmental crises there is selection for early sexual maturity at the level of the individual. So individuals who reach sexual maturity early are favored over individuals who reach sexual maturity late in life. Early maturer's due to their shorter generation time will become more numerous in the population over time. At the same time species with early maturing individuals are also fitter than species without such characteristics. Because the former are made up of individuals with short generation times, they tend to evolve rapidly and bud off new species. This type of species then becomes more numerous with time. Selection processes acting at the two levels, are complimentary. Unlike the earlier example I gave of the selfish gene where selection was favoring the cell containing the mutant gene but opposing the individual containing that gene.

After mass extinctions the nature and patterns of biotic recovery may depend on the characteristics of the survivor species. Selection can take place above the level of the individual. This species selection or species sorting as many people like to call it may lead to the establishment of long term macro-evolutionary patterns of the sort I described.


  1. Have you read Matt Ridley's book "The Red Queen: Sex and the Evolution of Human nature"? It applies the same logic to the way human brains and societies evolved. I am sure you will like it.

  2. Yes, Genome is one of my favorites in non-fiction.

  3. Is population size a factor?
    If a mass extinction event occurs and is followed by a period of rapid opportunistic genetic divergence into vacant niches (a la Darwin's Finches) then it would be advantageous to have as much diversity in the gene pool to draw on as possible. Bigger population more potential genetic permutations. Too small a population and less ability to evolve around a challenge but also less capacity to evolve into a vacant habitat?

  4. sure that would be a factor. but what types of organisms would more likely have larger population sizes? so a higher level control on population size might be small bodied species with faster generation times.