Network Structure and Selection Asymmetry Drive Coevolution in Species-Rich Antagonistic Interactions

Ecological interactions shape and are shaped by the evolution of interacting species. Mathematical models and empirical work have explored the multiple ways coevolution could occur in small sets of species, revealing that the addition of even one species can change the coevolutionary dynamics of a pairwise interaction. As a consequence, one of the current challenges in evolutionary biology is to understand how species-rich assemblages evolve and coevolve as networks of interacting species. We combined an adaptive network framework, a trait evolutionary model, and data on network structure to study how network organization affects and is affected by selection in antagonistic interactions such as parasitism, predation, and herbivory. We explored how selection imposed by interactions shapes the evolution of attack and defense traits, parameterizing our models with structural information from 31 empirical assemblages of antagonistic species. In the simulations, the form of coevolution in antagonistic interactions is affected by the intensity and asymmetry of the selection imposed by the interacting partners. Transient escalation in attack and defensive traits was the most prevalent form of coevolutionary dynamics, especially in networks formed by modules of highly interacting species. Fluctuating evolution of traits was observed when the intensity of selection was higher in exploiters than in victims and was especially favored in nested networks. At the species level, highly connected species experienced higher temporal variation in selection regardless of the network structure, resulting in high trait mismatching with their partners. The mismatched patterns of highly connected species, in turn, may explain the emergence of modularity in antagonistic interactions in which selection is stronger on exploiters than on their victims. Our results highlight the roles of different aspects of network structure on antagonistic coevolution: nestedness shapes coevolutionary dynamics, whereas modularity emerges as one outcome of coevolutionary dynamics.