Abstract
Exaggerated traits involved in species interactions have long captivated the imagination of evolutionary biologists and inspired the durable metaphor of the coevolutionary arms race. Despite decades of research, however, we have only a handful of examples where reciprocal coevolutionary change has been rigorously established as the cause of trait exaggeration. Support for a coevolutionary mechanism remains elusive because we lack generally applicable tools for quantifying the intensity of coevolutionary selection. Here we develop an approximate Bayesian computation (ABC) approach for estimating the intensity of coevolutionary selection using population mean phenotypes of traits mediating interspecific interactions. Our approach relaxes important assumptions of a previous maximum likelihood approach by allowing gene flow among populations, variable abiotic environments, and strong coevolutionary selection. Using simulated data, we show that our ABC method accurately infers the strength of coevolutionary selection if reliable estimates are available for key background parameters and ten or more populations are sampled. Applying our approach to the putative arms race between the plant Camellia japonica and its seed predatory weevil, Curculio camelliae, provides support for a coevolutionary hypothesis but fails to preclude the possibility of unilateral evolution. Comparing independently estimated selection gradients acting on Camellia pericarp thickness with values simulated by our model reveals a correlation between predicted and observed selection gradients of 0.941. The strong agreement between predicted and observed selection gradients validates our method.
Highlights
Few metaphors have captured the interest of evolutionary biologists and ecologists more than the coevolutionary arms race [1]
Exaggerated traits involved in species interactions, such as extreme running speeds in predator and prey, have long captivated the imagination of evolutionary biologists and inspired the durable metaphor of the coevolutionary arms race
Bayesian arms races applying the method to a well-studied interaction between the plant Camellia japonica and its seed predatory weevil, Curculio camelliae
Summary
Few metaphors have captured the interest of evolutionary biologists and ecologists more than the coevolutionary arms race [1]. The results of such studies can be consistent with a coevolutionary arms race (e.g., positive selection acting on putatively interacting host and pathogen genes), the degree of reciprocity between the species cannot be ascertained and alternative explanations for parallel positive selection are often plausible. As with the genetic approaches, these phenotypic studies can provide evidence consistent with a coevolutionary arms race (e.g., parallel patterns of trait escalation in the fossil record, correlated traits among populations, etc.), but are generally unable to quantify the extent of reciprocity or rule out alternative explanations for parallel patterns of escalation in interacting species. We are currently in a situation where we have tools that can be used to identify parallel patterns of genetic or phenotypic escalation in interacting species pairs, but few tools that can robustly estimate the degree of reciprocal or coevolutionary selection underlying these patterns of parallel evolutionary change
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