07 December 2010

Not all species interactions are (co)evolved equal

This post was chosen as an Editor's Selection for ResearchBlogging.orgBiologists have long thought that coevolutionary interactions between species help to generate greater biological diversity. This idea goes all the way back to The Origin of Species, in which Darwin proposed that natural selection generated by competition for resources helped cause species to diverge over time:
Natural selection, also, leads to divergence of character; for more living beings can be supported on the same area the more they diverge in structure, habits, and constitution, of which we see proof by looking at the inhabitants of any small spot or at naturalised productions.
—Darwin (1859), page 128.
In the twentieth century, this idea was extended into suggestions that coevolution between plants and herbivores or flowers and pollinators helped to generate the tremendous diversity of flowering plants we see today. In general, biologists have found that strong coevolutionary interactions are indeed associated with greater diversity.

Yet although there is a well-established association between coevolution and evolutionary diversification, correlation isn't causation. Furthermore, every species may coevolve with many others, and diversification that seems to be driven by one type of interaction might actually be better explained by another. It has even been suggested that coevolution rarely causes speciation at all.

Species interact in a lot of different ways, as antagonists, competitors, and mutualists. Do all these interactions shape diversity the same way? Photos by jby.
One step toward determining how often coevolution promotes diversification would be to identify what kinds of coevolutionary interaction are more likely to generate diversity. This is precisely the goal of a paper I've just published with Scott Nuismer in this month's issue of The American Naturalist. In it, we present a single mathematical model that compares a wide range of species interactions to see how they shape diversification, and that model shows that coevolution doesn't always promote diversity [PDF].

The model

The model considers two coevolving species that interact in many discrete populations linked by migration. The environment varies from population to population, and each population is finite, and so may be affected by genetic drift. The simulated critters reproduced in randomly-drawn pairs, with each pairing producing a single offspring whose trait value was the average of its parents', plus a small random effect to simulate mutation. These conditions mean that the two species would become more diverse even without coevolution—genetic drift and variable natural selection from the environment would both tend to increase diversity. Scott and I were interested in how coevolution changed this "baseline" diversification rate.

To do determine that, we allowed the two species to interact in a variety of different ways that mimic different kinds of real-world coevolutionary interactions. We then tracked the evolution of a single trait in each species that was necessary to the coevolutionary interaction, like a plant's anti-herbivore defenses, or a parasite's ability to infect its host, to see whether the trait became more diverse than expected without coevolution. By running these scenarios as computer simulations for hundreds of replicates, we could see what each kind of interaction did on average—a distribution of possible diversification. I'll discuss the specific results for three types of interactions.

Escalation

Escalation, or "arms race" dynamics, is what many people first think of when they think of evolution. In escalation interactions, each species benefits from having a trait that beats out the other species—plants that produce lots of defensive toxins, for instance, or prey with stronger shells to resist predators' jaws. Our simulations found that such interactions don't increase diversity in the two interacting species, as you can see from the graphic below.

When coevolution is mediated by "arms race" escalation, it results in about the same diversity that would evolve without coevolution. Image adapted from Yoder and Nusimer (2010).
The graphic shows two histograms, one overlaid on top of the other. The lower, green histogram shows the distribution of trait diversity, or phenotypic variance, values at the end of each of one thousand replicate simulations of escalation coevolution. The translucent white histogram shows the distribution of phenotypic variance values at the end of each of one thousand replicate simulations without any coevolution—and it almost exactly overlaps the green histogram. This means that escalation interactions do not tend to lead to greater diversity of the interacting trait. This occurred even though the species' traits "escalated," getting bigger over time—because phenotypes increased in every population, this arms race didn't result in more diversity among the populations.

Competition

Now consider competition over resources, as Darwin originally discussed. In this kind of species interaction, natural selection favors competitors that are less similar to each other—not necessarily bigger or smaller, just different. This kind of coevolution is thought to have contributed to the diversification of many different groups of organisms, including anole lizards on Caribbean islands. And in this case, our model found that coevolution boosted diversity quite a bit.

Competition causes many simulations to evolve greater diversity than they would without coevolution. Image adapted from Yoder and Nusimer (2010).
Many individual simulations ended up with more diversity than was seen in any of the simulations without coevolution—that long tail of orange sticking out from behind the white baseline distribution is a signal of greater diversification.

Mutualism

And what about mutualism, in which two interacting species benefit from being better matched to each other? This is the sort of coevolutionary selection apparently arising from the interaction of Joshua tree and its pollinators, which seem to be diverging in tandem. But when Scott and I simulated such an interaction, we found that it usually decreased diversity.

Mutualistic matching leads to less diversity than would otherwise evolve. Image adapted from Yoder and Nusimer (2010).
As you can see, the dark blue distribution of results is substantially narrower than the white baseline distribution, meaning that most simulations of mutualistic coevolution resulted in less phenotypic variance than would evolve in the absence of coevolution. It so happens that the latest analysis of Joshua trees and their pollinators [PDF] actually seems to confirm this prediction, but I'll discuss that result at a later date.

Coevolutionary selection isn't the whole story

In some respects these are surprising results—Scott and I found that some kinds of coevolutionary interaction that have been widely associated with greater diversity may actually have no effect on diversification, or act to reduce it. However, there are some caveats to consider in understanding our model. Specifically, we didn't simulate the actual formation of new species—just the evolution of diversity within species. It's possible that coevolutionary selection that acts to reduce diversity within species could actually make them more likely to form new species when some other force, like the creation of a geographic barrier, splits the species. I particularly think this is what's happened in the case of Joshua tree.

In fact, species interactions might often create new species indirectly in this fashion. For instance, plants with seeds evolved to be dispersed by ants seem to form new species more rapidly; but that's because ants are lousy seed dispersers, not because they create natural selection that directly forms new ant-dispersed plant species. Hopefully, this new model will help to differentiate these direct and indirect effects of coevolution on biological diversity.

References

Darwin, C. (1859). On the Origin of Species. London: John Murray. Full text on Google Books.

Godsoe, W., Yoder, J.B., Smith, C.I, Drummond, C., & Pellmyr, O. (2010). Absence of population-level phenotype matching in an obligate pollination mutualism J. Evol. Biology, 23 (12), 2739-46 DOI: 10.1111/j.1420-9101.2010.02120.x

Yoder, J., & Nuismer, S. (2010). When does coevolution promote diversification? The American Naturalist, 176 (6), 802-17 DOI: 10.1086/657048

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