Coevolutionary alternation in antagonistic interactions

Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844, USA.
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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    • "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.
    Ecology and Evolution 04/2013; 3(4):961-70. DOI:10.1002/ece3.518 · 2.32 Impact Factor
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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.
    Ecology Letters 09/2012; DOI:10.1111/ele.12010 · 10.69 Impact Factor
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    • "The Red Queen model stands out as a coevolutionary model because it does not primarily focus on fluctuating population densities, but rather on fluctuating genotype and phenotype frequencies of the interacting species. The causes and consequences of fluctuating genotype and phenotype frequencies in host-parasite, host-parasitoid and predator-prey interactions [4] are increasingly well understood at least in two-species systems, but direct empirical evidence of long-term dynamics is rare [5], not at least because long-term dynamics are inherently difficult to measure [6,7]. "
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    ABSTRACT: Background Antagonistic species interactions can lead to coevolutionary genotype or phenotype frequency oscillations, with important implications for ecological and evolutionary processes. However, direct empirical evidence of such oscillations is rare. The rarity of observations is generally attributed to inherent difficulties of ecological and evolutionary long-term studies, to weak or absent interaction between species, or to the absence of negative frequency-dependence. Results Here, we show that another factor – non-genetic inheritance, mediated for example by epigenetic mechanisms – can completely eliminate oscillations in the presence of such negative frequency dependence, even if only a small fraction of offspring are affected. We analytically derive the threshold value of this fraction at which the dynamics change from oscillatory to stable, and investigate how selection, mutation and generation times differences between the two species affect the threshold value. These results strongly suggest that the lack of phenotype frequency oscillations should not be attributed to the lack of strong interactions between antagonistic species. Conclusions Given increasing evidence of non-genetic effects on the outcomes of antagonistic species interactions, we suggest that these effects should be incorporated into ecological and evolutionary models of interacting species.
    BMC Evolutionary Biology 06/2012; 12(1):93. DOI:10.1186/1471-2148-12-93 · 3.37 Impact Factor
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