American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

Symposium: “How does co-evolution of consumer traits affect resource specialization?”

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Paula Vasconcelos and Claus Rueffler (Feb 2020)

How does joint evolution of consumer traits affect resource specialization? Hint: it’s more complicated than you think!

Read the Article (Just Accepted)

Simulation run showing evolutionary trajectory in trait space. The <i>x</i>-axis shows the trait for consumer’s feeding efficiency, and the <i>y</i>-axis shows the trait for consumer’s handling time. The point (0,0) represents a specialist for resource 1 and the point (1,1) represents a specialist for resource 2. Colors indicate the passage of time, where blue represents <i>t</i>&nbsp;=&nbsp;0 and dark red represents <i>t</i>&nbsp;=&nbsp;1&nbsp;000&nbsp;000.<br/><br/><br />(Credit: Paula Vasconcelos and Claus Rueffler)
Simulation run showing evolutionary trajectory in trait space. The x-axis shows the trait for consumer’s feeding efficiency, and the y-axis shows the trait for consumer’s handling time. The point (0,0) represents a specialist for resource 1 and the point (1,1) represents a specialist for resource 2. Colors indicate the passage of time, where blue represents t = 0 and dark red represents t = 1 000 000.
(Credit: Paula Vasconcelos and Claus Rueffler)

When should we expect the evolution of different resource specialists instead of a single generalists? To simplify the analysis, mathematical models addressing this question are usually based on the assumption of a single evolving consumer trait (think beak size in birds), which led to a pleasingly simple prediction: the evolution of resource specialists is favored by strong trade-offs (where resource generalists perform relatively poorly compared to specialists) while weak trade-offs (where resource generalists perform relatively well) favor the evolution of generalists. However, the assumption of a single evolving consumer trait is not realistic since organisms are complex and the interaction between consumers and their resources is affected by many jointly evolving traits.

PhD student Paula Vasconcelos and her supervisor Claus Rueffler from Uppsala University set out to investigate how evolutionary predictions are altered if two or three consumer traits were allowed to jointly evolve. They find that the simple dichotomy suggested by models based on a single evolving trait does not hold true in this more general setting. Instead, weak trade-offs can lead to either one or two specialists, as well as to a single generalist. The reason for these deviating results is that jointly evolving traits can interact in complicated ways in their effect on resource consumption. The results serve as a warning that simplifying assumptions—in this case, that the degree of resource specialization depends on a single trait—must be made carefully, and the results of models that use them should be qualified if the effects of violating these assumptions is unknown.

This study touches on another important question in biology: does complexity, as measured in number of jointly evolving traits, facilitates diversification? Surprisingly, the results show that complexity is in fact not a good predictor of diversifying potential as the conditions leading to two specialists are not necessarily more likely to be fulfilled when increasing the number of jointly evolving traits.


Abstract

Consumers regularly experience trade-offs in their ability to find, handle and digest different resources. Evolutionary ecologists recognized the significance of this observation for the evolution and maintenance of biological diversity long ago and continue to elaborate on the conditions under which to expect one or several specialists, generalists or combinations thereof. Existing theory based on a single evolving trait predicts that specialization requires strong trade-offs such that generalists perform relatively poorly, while weak trade-offs favor a single generalist. Here, we show that this simple dichotomy does not hold true under joint evolution of two or more foraging traits. In this case, the boundary between trade-offs resulting in resource specialists and resource generalists is shifted toward weaker trade-off curvatures. In particular, weak trade-offs can result in evolutionary branching leading to the evolution of two coexisting resource specialists while the evolution of a single resource generalist requires particularly weak trade-offs. These findings are explained by performance benefits due to epistatic trait interactions enjoyed by phenotypes that are specialized in more than one trait for the same resource.