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Frontiers in ZoologyOpen Access HypothesisAsymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie Laurent Lapchin* and Thomas Guillemaud Address: "Biologie des Populations en Interaction", UMR 1112 "Réponse des Organismes aux Stress Environnementaux", Inra/Unsa, 400 route des Chappes, BP167 06903 Sophia-Antipolis cedex, France Email: Laurent Lapchin* -lapchin@antibes.inra.fr; Thomas Guillemaud -guillem@antibes.inra.fr * Corresponding author AbstractBackground: Coevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species.Presentation of the hypothesis: When more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race. Testing the hypothesis:We propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization. Implications of the hypothesis:Genetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.

Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants

“…Meanwhile, the hosts showed high intraspecific variation in their responses to these phorid parasitoids, although the responses were similar among ant species and genera. This supports, at least in part, the asymmetry hypothesis proposed for parasitoid-host interactions (Lapchin 2002; Lapchin and Guillemaud 2005), according to which the parasitoids evolve specialized behaviors as they are able to select which host to attack, but the hosts acquire generalized responses against different parasitoid species since they are not capable of predicting which parasitoid species will attack them.…”

In silico Evolution of Lysis-Lysogeny Strategies Reproduces Observed Lysogeny Propensities in Temperate Bacteriophages

“…Here, we explore an alternate scenario where the lysogeny propensity is determined by competition between phage variants for the same bacterial host. Because bacteriophage DNA mutates at a relatively high rate (Drake, 1991 ), phage regulatory circuits can be easily tuned for different lysogenization propensities and adapt rapidly to new conditions and co-evolving bacteria (Lapchin and Guillemaud, 2005 ; Vos et al, 2009 ). For example, studies in lambda phage and P22 phage have revealed specific mutations in the phage genome—both in regulatory regions as well as coding regions of phage genes—that result in changes in the lysogeny propensity (Kaiser, 1957 ; Levine, 1957 ; Kourilsky, 1973 ; Gottesman and Weisberg, 2004 ; Schubert et al, 2007 ).…”

Parasitoid wasps influence where aphids die via an interspecific indirect genetic effect

“…Both selection and the genetic component of the phenotypes under selection become products of the interacting genotypes [9,10,22,25]. However, while the phenotype may be shared, there is an important asymmetry for understanding the evolutionary consequences of the parasitoid-host interaction [26]. For instance, parasitoids may have more choice of their aphid hosts than aphids have choice of their parasitoid attacker.…”