Mud time capsules show evolutionary arms race between host and parasite

This is the fifth of eight posts on evolutionary research to celebrate Darwin's bicentennial.


Blogging on Peer-Reviewed ResearchLife can sometimes be a futile contest. Throughout the natural world, pairs of species are locked in an evolutionary arms race where both competitors must continuously evolve new adaptations just to avoid ceding ground. Any advantage is temporary as every adaptive move from a predator or parasite is quickly neutralised by a counter-move from its prey or host. Coerced onward by the indifferent force of natural selection, neither side can withdraw from the stalemate.

i-33db9d5cd6c706fa474a4cd297e63b5c-daphnia_magna01.jpgThese patterns of evolution are known as Red Queen dynamics, after the character in Lewis Carroll's Through the Looking Glass who said to Alice, "It takes all the running you can do, to keep in the same place." These arms races are predicted by evolutionary theory, not least as an explanation for sex. By shuffling genes from a mother and father, sex acts as a crucible for genetic diversity, providing a species with the raw material for adapting to its parasites and keep up with the arms race.

We can see the results of Red Queen dynamics in the bodies, genes and behaviours of the species around us but actually watching them at work is another matter altogether. You'd need to study interacting species over several generations and most biologists have neither the patience nor lifespan to do so. But sometimes, players from generations past leave behind records of the moves they made. Ellen Decaestecker and colleagues from Leuven University found just such an archive in the mud of a Belgian lake.

The lake is home to a small crustacean called a water flea (Daphnia magra) and a parasitic bacteria Pasteuria ramosa that lives inside it. Both species can undergo dormant states, and Decaestecker found that the lake's sediment preserves members of this sleeping fauna from up to 39 years ago. Every layer of sediment acts as a time capsule, preserving members from previous generations

Decaestecker sampled cylinders of sediment form the lake and revived dormant Daphnia eggs and parasite spores from different levels, representing intervals of 2-4 years. With these, she managed to hatch living Daphnia and pit them against parasites from their past, present and future.

On average, she found that the bacteria infected the water fleas more successfully if they came from the same time period than if they hailed from the past. As time went on, the bacteria picked up new adaptations that made them more effective parasites.

But Decaestecker also found that bacteria from a flea's future were also less infectious than its contemporaries. It seems that the parasites' upper hand is short-lived for the fleas evolve their own counter-adaptations. As the bacteria continue to adapt to the changing defences of their hosts, they trade-off the ability to infect the current generation with their ability to infect the previous ones.

This particular race isn't quite as one-sided as it might appear for slowly. Over time, the bacteria didn't become any better at infecting the water fleas, but those that did caused more virulent disease. They produced more reproductive spores and millions of these take up the fleas' bodies and effectively castrate them. Over time, the reproductive success of the infected fleas fell.

Reference: Decaestecker, E., Gaba, S., Raeymaekers, J.A., Stoks, R., Van Kerckhoven, L., Ebert, D., De Meester, L. (2007). Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature, 450(7171), 870-873. DOI: 10.1038/nature06291

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The arms race analogy isn't entirely apt because the parasite needs the host to reproduce and the predator needs prey to reproduce. Otherwise we get what humans have done--overfishing, for example, to the point of extinction. If the predator developed an unbeatable mechanism for attacking prey, then subsequent generations would starve, no?

This seems to be in exact agreement with Hamilton's theory of the role of parasites in the evolutionary maintenance of sex. See "Narrow Roads of Gene Land", his amazing collected works. It is not really true that sex increases diversity: rather, as Hamilton's simulations showed, it allows the preservation of once and-future anti-parasite strategies that are temporarily useless in the cycle. Gradual improvement of strategies (plural) happens at a much slower scale than the fast evolutionary scale of the parasite. Very exciting confirmation of the theory, in fact! (Current views are that this is not the whole role of sex; still, it seems to be a major factor.)

Intrigued by Lilian's comment. Is that a prediction that evolutionary theory can make. That we should find examples of predators/parasites wiping out their prey/host populations because a mutated mechanism makes them unbeatable?

I would be careful about saying that any mutation is "unbeatable". Not that you did, but others have in the past and it's often a failure of imagination. As Lesley Orgel put it, "Evolution is cleverer than you.".

That being said, here's an example of a predator/prey relationship, where some populations of predators appear to have temporarily won the arms race. Note that I say temporarily. Also note that in this case, prey defence might not limit individual predators but prey population size will limit predator population size. The seemingly invincible snakes are still restrained by the fact that if they eat all their prey, they won't have enough food, their numbers will fall, giving the newts a chance to rebound. And so on.

It seems a little Lamarckian to say that parasites and hosts evolve new adaptations in an arms race, is it not? A parasite invades a host and reproduces. Some members of that parasite species have the adaptations necessary to survive the onslaught of the immune system or other defense mechanism of the host, so they survive and reproduce, making it more likely that their offspring will live--as long as they don't kill the host species. The host species' members with the adaptations necessary to survive the onslaught of the parasitic invation will survive to reproduce, making their offspring more likely to survive, as well. What happens over time is that the two species will become more specialized and dependent on each other, and any adaptation that makes it more likely for some of one or the other species to die makes it certain that only particular members of each species will survive to reproduce. That's why past and future parasites cannot be successful in present hosts; they are specialized to survive in a host with particular adaptations because of the adaptations they have themselves. Parasites tend to survive because of rapid reproduction, which tends to make their genetic variation more rapid, as well, since some genes are added with each generation. It's not likely that parasites will go away in a given host species, regardless of the rapidity of host variation.

Species go extinct all the damn time. Can't parasite pressure be a factor, even a major factor, or even the factor, in an extinction? Is there any inherent natural limit on how damaging a parasite's innovation may be? That we don't notice this much must be selection bias: we mostly see processes that last, and most of the sudden extinctions (that we didn't arrange ourselves!) happened before we came along.

Furthermore, parasites/predators can often switch to another, possibly less hospitable, host if they eliminate the present favorite, so their numbers need not decline as fast as their prey's. Finally, a very few remaining exclusive predators may suffice to finish off the prey population if it reproduces slowly enough.

For copious examples of extinction by predation, examine any Pacific island. For near-historical drama, consider humans vs. the passenger pigeon.

Sometimes arms races are won, and sometimes the victory is Pyrrhic.

By Nathan Myers (not verified) on 11 Feb 2009 #permalink