Evolution of camouflage drives rapid ecological change in an insect community

Evolutionary change in individual species has been hypothesized to have far-reaching consequences for entire ecological communities, and such coupling of ecological and evolutionary dynamics (“eco-evolutionary dynamics”) has been demonstrated for a variety systems. However, the relative importance of evolutionary dynamics for ecological dynamics remains unclear. Here, we investigate how spatial patterns of local adaptation in the stick insect Timema cristinae, driven by natural selection, gene flow and founder effects, structure metapopulations, communities, and multitrophic interactions.

Observations of a wild T. cristinae metapopulation show that locally imperfect camouflage reduces population size, and that the effect of such maladaptation is comparable to the effects of more traditional ecological factors, including habitat patch size and host-plant species identity. Field manipulations of local adaptation and bird predation support the hypothesis that maladaptation reduces population size through an increase in bird predation. Furthermore, these field experiments show that maladaptation in T. cristinae and consequent increase in bird predation reduce the pooled abundance and species richness of the co-occurring arthropod community, and ultimately cascade to decrease herbivory on host plants. An eco-evolutionary model of the observational data demonstrates that the demographic cost of maladaptation decreases habitat patch occupancy by T. cristinae but enhances metapopulation-level adaptation.

The results demonstrate a pervasive effect of ongoing evolution in a spatial context on population and community dynamics. The eco-evolutionary model generates testable predictions about the influence of the spatial structure of the patch network on the abundance and adaptive camouflage evolution.