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

Abstract

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.

Novel interactions between alien pathogens and native plants increase plant–pathogen network connectance and decrease specialization

“…By contrast, the native network was highly specialized and modular, consistent with theoretical expectations for plants and pathogens with a long shared evolutionary history (Andreazzi et al, 2017;Lewinsohn & Prado, 2006). Modularity in our native network was higher than in other published plant-pathogen networks (Barrett, Encinas-Viso, Burdon, & Thrall, 2015) and many other high-intimacy networks (Pires & Guimarães Jr, 2012).…”

“…Identifying modules and understanding their composition can provide insight into why and how host plants share pathogens (Lewinsohn & Prado, 2006). In plant-pathogen networks, modules are often correlated with host phylogeny when groups of related plant species tend to be colonized by a shared suite of pathogens TA B L E 1 A brief description of common metrics that describe network architecture and function and the predicted relative values of these metrics in networks of novel interactions, as compared with the metrics in non-novel networks (Andreazzi et al, 2017) (Elias, Fontaine, & van Veen, 2013;Vacher, Piou, & Desprez-Loustau, 2008). We expect module composition in novel native plant-alien pathogen networks to show a strong signal of host phylogeny if alien pathogens are pre-adapted to colonize novel hosts in the new range that are closely related to hosts from the pathogen's native range (Bufford et al, 2016;Gilbert, Magarey, Suiter, & Webb, 2012;Parker et al, 2015).…”

Tri‐trophic interactions: bridging species, communities and ecosystems

“…terHorst et al ) and applying network analyses to understand how community structure affects the evolution of component interactions (e.g. Andreazzi et al ).…”

The global structure of marine cleaning mutualistic networks

“…A persistent challenge in ecology is to unravel the interplay between ecological and evolutionary processes shaping these interactions. Recent years have seen a surge in the study of the resultant ecological networks, aiming to disentangle the underlying drivers of their structure (e.g., Andreazzi, Thompson, & Guimarães, ; Bascompte, Jordano, Mélián, & Olesen, ; Fontaine et al, ) and reveal the implications of this structure for individual fitness, population structure and community dynamics (e.g., Bascompte & Jordano, ; Pascual & Dunne, ). Although the bulk of the work comes from studies at the local community scales, the latest research has been tackling the timely challenge of assessing general assembling principles of ecological networks at large spatial scales (e.g., Martín‐González et al, ; Zanata et al, ).…”