Camouflage evolutionary dynamics structure plant-arthropod communities
The role of rapid evolution in driving patterns of community structure is beginning to gain widespread acknowledgement from ecologists and evolutionary biologists alike. However, theoretical advances are now severely outpacing empirical demonstrations of such “eco-evolutionary” effects. Furthermore, these empirical demonstrations largely focus on how evolution by natural selection can influence communities, categorically ignoring the effects of other fundamental evolutionary processes, such as gene flow.
We investigated the role of interactions between natural selection and gene flow on plant-arthropod communities by focussing on variation in the degree of camouflage (mal)adaptation in the Californian stick insect Timema cristinae. To do so, we coupled field manipulations with observations, addressing both causation and relevance of maladaptation for plant-arthropod communities. In two field experiments, we manipulated maladaptation by transplanting wild-caught individuals of different phenotypes to wild host plants and examined effects on T. cristinae recapture rate, non-Timema arthropod abundance and diversity, as well as rates of non-Timema herbivory. In two observational studies, we correlated natural variation in maladaptation with similar measures of population and community structure.
The field experiments strongly demonstrate that maladaptation in camouflage can influence reduce the abundance of T. cristinae, the abundance and diversity of non-Timema arthropods, as well as the rate of non-Timema herbivory. Furthermore, we show that these effects are due to an increase in the strength of bird predation in response to poor camouflage. Field observations show less clear results, but generally corroborate our experimental findings. We report smaller natural T. cristinae population sizes where they are poorly camouflaged, and the magnitude of these effects was high. Experimental R-square values for the influence of maladaptation ranged from 0.12 and 0.50, and the effect of maladaptation on T. cristinae population size in nature showed an R-square of 0.07, comparable to the effects of traditional ecological variables, such as habitat patch size (0.14) and host-plant species identity (0.05).
Our results add to a growing body of research demonstrating that rapid evolutionary dynamics can substantially influence ecological patterns at multiple levels of biological organization. Furthermore, we add to this literature that gene flow, through its role in constraining local adaptation, can be an important evolutionary process influencing ecology, alongside natural selection. As epidemiologists and agricultural researchers have known for decades, incorporating the potential for rapid evolution into an ecological worldview is necessary to a complete understanding of nature and the ability to exert control over it.