Antagonistic Coevolution Mediated by Phenotypic Differences Between Quantitative Traits

Nuismer, Scott L.; Ridenhour, Benjamin J.; Oswald, Benjamin P.

doi:10.1111/j.1558-5646.2007.00158.x

Cited by 61 publications

(89 citation statements)

References 60 publications

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“…The chief alternative to antagonistic arms races is the 'phenotype matching' model, where one coevolutionary participant benefits from a match to a second participant's phenotype, while this second participant benefits from a mismatch [9]. Therefore, the degree of matching, and not the difference between trait values, decides the fitness outcomes when two individuals meet.…”

Section: Introductionmentioning

confidence: 99%

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Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

2016

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Measuring local adaptation can provide insights into how coevolution occurs between predators and prey. Specifically, theory predicts that local adaptation in functionally matched traits of predators and prey will not be detected when coevolution is governed by escalating arms races, whereas it will be present when coevolution occurs through an alternate mechanism of phenotype matching. Here, we analyse local adaptation in venom activity and prey resistance across 12 populations of Northern Pacific rattlesnakes and California ground squirrels, an interaction that has often been described as an arms race. Assays of venom function and squirrel resistance show substantial geographical variation (influenced by site elevation) in both venom metalloproteinase activity and resistance factor effectiveness. We demonstrate local adaptation in the effectiveness of rattlesnake venom to overcoming present squirrel resistance, suggesting that phenotype matching plays a role in the coevolution of these molecular traits. Further, the predator was the locally adapted antagonist in this interaction, arguing that rattlesnakes are evolutionarily ahead of their squirrel prey. Phenotype matching needs to be considered as an important mechanism influencing coevolution between venomous animals and resistant prey.

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Section: Introductionmentioning

confidence: 99%

“…[9]), and should be distinguished from 'trait matching' at the population level, where the population-mean trait values of two interacting species are positively correlated (e.g. [3,4,12]).…”

Section: Introductionmentioning

confidence: 99%

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

2016

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“…We further assume that these interspecific interactions among A, B, andB are governed by a single quantitative trait in each species (z A, z B , and zB, respectively). Encounters between individuals of different species have fitness consequences that depend on either the absolute (phenotype matching) or signed (phenotype differences) distance between their trait values (22)(23)(24).…”

Section: Model and Analysismentioning

confidence: 99%

Revisiting Darwin's conundrum reveals a twist on the relationship between phylogenetic distance and invasibility

Jones

Nuismer

Gomulkiewicz³

2013

Proc. Natl. Acad. Sci. U.S.A.

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A key goal of invasion biology is to identify the factors that favor species invasions. One potential indicator of invasiveness is the phylogenetic distance between a nonnative species and species in the recipient community. However, predicting invasiveness using phylogenetic information relies on an untested assumption: that both biotic resistance and facilitation weaken with increasing phylogenetic distance. We test the validity of this key assumption using a mathematical model in which a novel species is introduced into communities with varying ecological and phylogenetic relationships. Contrary to what is generally assumed, we find that biotic resistance and facilitation can either weaken or intensify with phylogenetic distance, depending on the mode of interspecific interactions (phenotype matching or phenotype differences) and the resulting evolutionary trajectory of the recipient community. Thus, we demonstrate that considering the mechanisms that drive phenotypic divergence between native and nonnative species can provide critical insight into the relationship between phylogenetic distance and invasibility.nvasive species are a major cause of concern due to their large ecological, social, and economic consequences (1-3). In principle, future invasions could be avoided by preventing introductions of potential invaders into susceptible communities. Thus, research has focused on identifying the characteristics that predispose species to becoming invasive (4-7) and the properties that make communities susceptible to invasion (8, 9). Although generalities have been elusive, one approach that has recently been gaining interest is using phylogenetic distance (time since cladogenesis) between nonnative species and species in the recipient community as an indicator of invasion potential.Darwin was the first to suggest that the probability of establishment by introduced species depends on their relatedness to native species (10). However, as Darwin noted, the ecological similarity of related species can have opposing effects on their potential for coexistence ("Darwin's naturalization conundrum"). On the one hand, establishment in regions with close relatives should be facilitated by favorable abiotic conditions and the presence of suitable prey, hosts, and mutualists (Fig. 1A). On the other hand, establishment in these regions should be inhibited by competition with the relatives themselves and exploitation by shared natural enemies (Fig. 1B). Citing observations by Alphonse de Candolle and Asa Gray that naturalized species are more frequently from nonnative genera, Darwin concluded that competition was the dominant factor and relatedness to native species should reduce establishment success ("Darwin's naturalization hypothesis").However, recent studies using statistical models, molecular phylogenetics, and experimental community assembly have revealed that the correlation between relatedness and establishment probability can be positive, negative, or zero (Table 1). These findings call into question the paramoun...

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“…Levels of reciprocal selection within and across patches could be seen as indicators of specialization, since strong local reciprocal selection can initiate the divergence of a single generalist into multiple specialists [18]. Links between reciprocal selection and specificity will be influenced by the availability of novel genotypes via mutation or migration [19], drift (although its impact is expected to be weak if reciprocal selection is strong), trait matching [20] and trade-offs with other fitness-determining traits [21]. A central prediction of coevolutionary theory is that, in tightly coupled associations, the strength of frequency-dependent cycles will depend on the degree of specialization in interacting genotypes [22], or cost-based trade-offs leading to fixed host ranges [23], the latter being consistent with a multi-locus gene-for-gene interaction.…”

Section: Introductionmentioning

confidence: 99%

Trophic network structure emerges through antagonistic coevolution in temporally varying environments

2011

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Understanding the mechanisms underlying ecological specialization is central to our understanding of community ecology and evolution. Although theoretical work has investigated how variable environments may affect specialization in single species, little is known about how such variation impacts bipartite network structure in antagonistically coevolving systems. Here, we develop and analyse a general model of victim -enemy coevolution that explicitly includes resource and population dynamics. We investigate how temporal environmental heterogeneity affects the evolution of specialization and associated community structure. Environmental productivity influences victim investment in resistance, which will shape patterns of specialization through its regulating effect on enemy investment in infectivity. We also investigate the epidemiological consequences of environmental variability and show that enemy population density is maximized for intermediate lengths of productive seasons, which corresponds to situations where enemies can evolve higher infectivity than victims can evolve defence. We discuss our results in the light of empirical studies, and further highlight ways in which our model applies to a range of natural systems.

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Antagonistic Coevolution Mediated by Phenotypic Differences Between Quantitative Traits

Cited by 61 publications

References 60 publications

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

Revisiting Darwin's conundrum reveals a twist on the relationship between phylogenetic distance and invasibility

Trophic network structure emerges through antagonistic coevolution in temporally varying environments

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