Coevolutionary alternation in antagonistic interactions

Department of Ecology & Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, California, United States
Evolution (Impact Factor: 4.61). 12/2006; 60(11):2207-17. DOI: 10.1111/j.0014-3820.2006.tb01858.x
Source: PubMed


Coevolution between parasites and hosts or predators and prey often involves multiple species with similar kinds of defenses and counter-defenses. Classic examples include the interactions between phytophagous insects and their host plants, thick-shelled invertebrates and their shell-crushing predators, and ungulates and their predators. There are three major hypotheses for the nonequilibrium coevolutionary dynamics of these multispecific trophic interactions: escalation in traits, cycles in traits leading to fluctuating polymorphisms, and coevolutionary alternation. The conditions under which cycles and escalation are likely to occur have been well developed theoretically. In contrast, the conditions favoring coevolutionary alternation-evolutionary fluctuations in predator or prey preference driven by evolutionary shifts in relative levels of prey defense and vice versa-have yet to be identified. Using a set of quantitative coevolutionary models, we demonstrate that coevolutionary alternation can occur across a wide range of biologically plausible conditions. The result is often repeated, and potentially rapid, evolutionary shifts in patterns of specialization within networks of interacting species.

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    • "In the case of no correlation (independent predator effects), the combined effect of multiple predators may result in divergent selection for specialist defence strategies, where different sub-populations adapt to different interacting species (Futuyma and Moreno, 1988; Davies and Brooke, 1989; Nuismer and Thompson, 2006; Edeline et al., 2008). If defence correlations are negative, selection by one predator could reduce the selection imposed by another predator owing to trade-offs in morphology or physiology (Davies and Brooke, 1989; Stinchcombe and Rausher, 2001; Thompson and Cunningham, 2002; Nuismer and Thompson, 2006; Berenbaum and Zangerl, 2006; Friman and Buckling, 2013). It is also possible that defence against one predator correlates positively with the defence against other predator (for example, owing to functional similarity between different enemies). "
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    ABSTRACT: Community dynamics are often studied in subsets of pairwise interactions. Scaling pairwise interactions back to the community level is, however, problematic because one given interaction might not reflect ecological and evolutionary outcomes of other functionally similar species interactions or capture the emergent eco-evolutionary dynamics arising only in more complex communities. Here we studied this experimentally by exposing Pseudomonas fluorescens SBW25 prey bacterium to four different protist predators (Tetrahymena pyriformis, Tetrahymena vorax, Chilomonas paramecium and Acanthamoeba polyphaga) in all possible single-predator, two-predator and four-predator communities for hundreds of prey generations covering both ecological and evolutionary timescales. We found that only T. pyriformis selected for prey defence in single-predator communities. Although T. pyriformis selection was constrained in the presence of the intraguild predator, T. vorax, T. pyriformis selection led to evolution of specialised prey defence strategies in the presence of C. paramecium or A. polyphaga. At the ecological level, adapted prey populations were phenotypically more diverse, less stable and less productive compared with non-adapted prey populations. These results suggest that predator community composition affects the relative importance of ecological and evolutionary processes and can crucially determine when rapid evolution has the potential to change ecological properties of microbial communities.
    Full-text · Article · Jan 2016 · The ISME Journal
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    • "Although coevolutionary alternation with escalation was defined as enemies shifting from one victim species to another (Thompson 2005), the same underlying process could occur with shifts between different populations of victims. In the model of coevolutionary alternation (without escalation; Nuismer and Thompson 2006), the predator or parasite specializes on one victim species at a time so that defenses decline in past victim species. This would presumably arise because trade-offs favor specialization on only one or a few victim species at a time. "
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    ABSTRACT: Although we often focus on the causes of geographic variation, understanding processes that act to reduce geographic variation is also important. Here, we consider a process whereby adaptive foraging across the landscape and directional selection exerted by a conifer seed predator, the common crossbill (Loxia curvirostra), potentially act to homogenize geographic variation in the defensive traits of its prey. We measured seed predation and phenotypic selection exerted by crossbills on black pine (Pinus nigra) at two sites in the Pindos Mountains, Greece. Seed predation by crossbills was over an order of magnitude higher at the site where cone scale thickness was significantly thinner, which was also the cone trait that was the target of selection at the high predation site. Additional comparisons of selection differentials demonstrate that crossbills exert selection on black pine that is consistent in form across space and time, and increases in strength with increasing seed predation. If predators distribute themselves in relation to the defensive traits of their prey and the strength of selection predators exert is proportional to the amount of predation, then predators may act to homogenize trait variation among populations of their prey in a process analogous to coevolutionary alternation with escalation.
    Full-text · Article · Apr 2013 · Ecology and Evolution
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    • "However, it remains unclear to what extent defence to one enemy directly reduced defence to the other. The evolution of specialised resistance is crucial to the maintenance of pairwise coevolutionary interactions at the community level (Nuismer & Thompson 2006). But why did bacteria diversify in their resistance strategies rather than evolving generalised defence? "
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    ABSTRACT: The impact of community complexity on pairwise coevolutionary dynamics is theoretically dependent on the extent to which species evolve generalised or specialised adaptations to the multiple species they interact with. Here, we show that the bacteria Pseudomonas fluorescens diversifies into defence specialists, when coevolved simultaneously with a virus and a predatory protist, as a result of fitness trade-offs between defences against the two enemies. Strong bacteria-virus pairwise coevolution persisted, despite strong protist-imposed selection. However, the arms race dynamic (escalation of host resistance and parasite infectivity ranges) associated with bacteria-virus coevolution broke down to a greater extent in the presence of the protist, presumably through the elevated genetic and demographic costs of increased bacteria resistance ranges. These findings suggest that strong pairwise coevolution can persist even in complex communities, when conflicting selection leads to evolutionary diversification of different defence strategies.
    Full-text · Article · Sep 2012 · Ecology Letters
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