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1 March 2006 Evolution for the Community Ecologist
RAGAN M. CALLAWAY
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The Geographic Mosaic of Coevolution. John N. Thompson. University of Chicago Press, Chicago, 2005. 400 pp. $28.00 (ISBN 0226797627 paper).

With the exception of consumer–prey interactions, the study of ecological communities has resisted efforts to integrate evolution into its theoretical foundations. John Thompson's The Geographic Mosaic of Coevolution takes a leap toward solving this problem and dramatically expands the evolutionary framework for other ecological subdisciplines. Thompson's latest contribution joins forces with rapidly expanding research (e.g., Stinchcombe and Rausher 2001, 2002) demonstrating that the magnitude or direction of natural selection on traits that mediate interactions between species is strongly affected by the presence of other community members.

Ecologists, and in particular community ecologists, should read this book. I make this recommendation from the perspective of an evolutionarily challenged community ecologist, one who found in Thompson's book exceptionally thought-provoking arguments and evidence for biotically driven evolutionary relationships among species, and for the importance of spatial and temporal conditionality of these relationships. Conditional interactions among species are a focal point in community ecology, and Thompson's articulate integration of ecological conditionality into community evolution made me rethink and reorganize my own perspectives on the natural world. Perhaps evolutionary sophisticates will be much more familiar with the arguments in The Geographic Mosaic of Coevolution, but for ecologists focused on the importance of species interactions to the conceptual issues of community theory, the book is a wealth of new ideas. Not only will pondering the geographic mosaic affect the way we think about evolution, it will affect the way we think about the processes that determine the distribution and abundance of species.

Exceptionally clear and well written, the arguments for the geographic mosaic of coevolution struck me as a babushka doll, the outer shell composed of repeated, relentless emphasis on the primary message: “Natural selection on interspecific interactions varies among populations partly because there are geographic differences in how fitness in one species depends on the distribution of genotypes in another species.” (The repetition is effective: I got the message.)

The second layer is a well-organized outline of the basic conceptual components of the geographic mosaic theory, presented in two parts. In part 1, “The Framework of Coevolutionary Biology,” chapter topics include raw materials for coevolution, local adaptation, and coevolutionary diversification. In part 2, “Specific Hypotheses on the Classes of Coevolutionary Dynamics,” the main topics are antagonistic and mutualistic interactions and coevolutionary displacement.

The innermost layer is a comprehensive presentation of an amazing number of empirical examples for the framework and hypotheses. Thompson shows both breadth and depth in his choice of those examples, and his simple style of explanation makes the important concepts that they illustrate accessible to the nonspecialist.

Die-hard anticoevolutionists may be disappointed that Thompson mostly ignores old arguments about undeniable proof for coevolution and bases his epistemology on relationships among species that are difficult to explain in any way but coevolution. However, those who get past their disappointment will have the opportunity to contemplate novel ideas about evolution and ecology.

While the coevolutionary process Thompson details is fascinating and wonderful, the explicit theory for a geographical nature of any biotically driven evolution brings new excitement to community ecology. Conditionality in community interactions may actually mean something. Spatial conditionality in species interactions appears to almost always drive divergence in evolutionary trajectories, which may feed back to community organization in ways that this book makes clear. Moreover, evidence showing that evolutionary relationships among pairs of species can be altered by the presence of other species brings new light to the contentious subject of community evolution. Thompson implicitly recognizes that the value of the geographic mosaic goes beyond strict co-evolution (“not all interactions are tightly coevolved”), and that greater knowledge of past, present, and future interdependence among species contributes to a better understanding of the processes that form communities.

As someone who is particularly interested in plants, I was curious about the paucity of examples involving interactions among plants. Thompson missed some important studies of plant interactions that vary in a geographically explicit manner (for example, the work of Roy Turkington and Lonnie Aarssen), others that have strong implications for evolved variation in plant interactions, and at least one theoretically relevant paper, but it is the dearth of extant relevant literature on the evolutionary nature of plant interactions that is especially intriguing. Even the simplest comparisons of competitive intensity among plant populations from different locations within their distributions would have been a major step toward understanding how plant interactions fit into the geographic mosaic concept. Integrating geographical mosaics into processes such as indirect competitive networks—see the discussion on page 329—would be profound. Clearly, exploring Thompson's ideas within plant communities is a major opportunity for future research.

Although my particular interest in the geographic mosaic theory is in its relevance and importance to community ecology, Thompson's fundamental goal is to squarely identify the process of co-evolution as a foundational biological principle. I think he succeeds. Old arguments against coevolution, based on the lack of irrefutable experimental proof of reciprocal evolutionary relationships—as if anything big in ecology or evolution were based on irrefutable proof—seem hollow in the light of carefully described evolutionary mosaics of crossbills and pine trees, parsnips and webworms, yucca moths and yuccas, toxic newts and resistant garter snakes, and hummingbirds and heliconias. New arguments for the importance of interspecific interactions, variation in their outcomes in different communities, and local adaptation of populations to each other are robust and compelling. Thompson's empirical examples and cogent arguments provide a new way to look at community ecology's past, but evidence that “reciprocal evolutionary change shapes interspecific interactions across continents and oceans and over time” points to its future.

References cited

1.

J. R. Stinchcombe and M. D. Rausher . 2001. Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea herecaea. American Naturalist 158:376–388. Google Scholar

2.

J. R. Stinchcombe 2002. The evolution of tolerance to deer herbivory: Modifications caused by the abundance of insect herbivores. Proceedings: Biological Sciences 269:1241–1246. Google Scholar

Appendices

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RAGAN M. CALLAWAY "Evolution for the Community Ecologist," BioScience 56(3), 266-267, (1 March 2006). https://doi.org/10.1641/0006-3568(2006)056[0266:EFTCE]2.0.CO;2
Published: 1 March 2006
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