Eco-evolutionary Island Biogeography

(This post is by Tim Farkas. I am just putting it up. Andrew)

If pressed to list the most influential paradigms of the last century, few ecologists would forget MacArthur and Wilson’s (1967) theory of island biogeography, and even fewer would intentionally exclude it. Since its inception, island biogeography has served as a powerful neutral model to explain patterns of biodiversity across space, and has seen its share of modifications, amendments, and criticisms, as befits any theory so prominent and enduring. Even when challenged to compete with metacommunity theory – its freshly minted and highly comprehensive contemporary – island biogeography performs surprisingly well, boasting a highly intuitive framework within which to develop new theory.

The late Robert H. MacArthur (left), a more recent E. O. Wilson, and their iconic 1967 book.

Perhaps it was only a matter of time, then, as the eco-evolutionary synthesis came into focus, that island biogeography was reconsidered in the light of rapid and ecologically powerful evolutionary dynamics. In the March issue of Trends in Ecology and Evolution, my colleagues and I (Farkas et al. 2015) point out that habitat area and isolation, central variables that influence equilibrium species richness in island biogeography theory (MacArthur and Wilson 1967), can also influence the fundamental processes of ecological genetics: gene flow, mutation, genetic drift, and natural selection. Hence, while area and isolation determine colonization and extinction rates through neutral processes, they can also cause rapid evolution.

MacArthur and Wilson’s (1967) original model. Small islands experience higher rates of extinction than larger islands, and isolated (far) islands experience less colonisation than well-connected islands (near), driving differences between islands in species richness at equilibrium.

We go on to lay down a general framework for how rapid evolution itself can influence equilibrium species richness, though effects on colonization and extinction. The key is that different evolutionary processes either promote or break down local adaptation, so habitat isolation and area can determine the location of a species on the “(mal)adaptation” continuum (Hendry and Gonzalez 2008). Building off the trophic theory of island biogeography (Gravel et al. 2011), (mal)adaptation in a single species can ripple through food webs and impact community-level patterns of colonization and extinction, ultimately influencing species richness at equilibrium.

The take-home: habitat area and isolation can have effects on equilibrium species richness mediated by both ecology and evolution, and those effects might reinforce or oppose one another.

Gene flow is perhaps the best process with which to illustrate eco-evolutionary island biogeography, because it is dependent on dispersal, which is heavily influenced by habitat isolation. A highly isolated habitat is expected to have low species richness at equilibrium, because colonization events will be rare, relative to a well-connected habitat (MacArthur and Wilson 1967). However, isolation will also reduce gene flow. Gene flow can have a diversity of consequences, but if gene flow is strong, and comes from populations locally adapted to divergent habitats, it breaks down local adaptation. Supposing gene flow causes local maladaptation, what may be predicted for colonization and extinction throughout the community? It depends on the role of the maladapted species in the food web. If maladaptation in a generalist pollinator reduces its abundance, the likelihood of extinction for plant mutualists might increase, reducing their species richness. On the other hand, if maladaptation reduces the abundance of a dominant consumer (e.g., a granivorous rodent), it could increase the species richness of competitors (other rodents).

In one of the examples above, the effects of isolation on species richness mediated by ecology and evolution oppose one another. In an extreme, where the evolutionary effect outweighs the ecological effect, isolated habitats could in theory have higher species richness than well-connected habitats, at least for particular guilds. This outcome can be illustrated using MacArthur and Wilson’s (1967) equilibrium figure of crossing extinction and colonization curves.

Reprinted from Farkas et al. (2015). Notice, in our extension of island theory, how an opposing influence of (mal)adaptation can lead to inverted predictions compared to island theory (arrows), such that highly connected patches have lower species richness at equilibrium (bottom). C = connected, I = isolated.

We draw three primary conclusions in this article. First, eco-evolutionary dynamics research would benefit from the explicit inclusion of gene flow, mutation, and genetic drift alongside natural selection. Second, a study of (mal)adaptation is likely a profitable means by which to accomplish that goal.  Third, rapid evolution can have a strong influence on species richness, and in particular can modify the core predictions of island biogeography. We hope this perspective encourages evolutionary ecologists to focus on (mal)adaptation and to incorporate evolutionary dynamics into their studies of biogeographic patterns. 

References

Farkas, T. E., A. P. Hendry, P. Nosil, and A. P. Beckerman. 2015. How maladaptation can influence biodiversity: Eco-evolutionary island biogeography. Trends in Ecology & Evolution 30.

Gravel, D., F. Massol, E. Canard, D. Mouillot, and N. Mouquet. 2011. Trophic theory of island biogeography. Ecology Letters 14:1010–1016.

Hendry, A. P., and A. Gonzalez. 2008. Whither adaptation? Biology & Philosophy 23:673–699.

MacArthur, R. H., and E. O. Wilson. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ.