Temperature alters specificity in a host-parasite interaction

The Red Queen Hypothesis proposes that genetic variation is maintained in populations through antagonistic coevolution of hosts and parasites. A major assumption of the Red Queen Hypothesis is tight genetic specificity for infection. However, it has been argued that this genetic interaction of host and parasite (G_HxG_P) is sensitive to environmental context (G_HxG_PxE). Environmental change could accordingly disrupt coevolutionary oscillations on relevant time scales, calling into question antagonistic coevolution as a general and robust explanation for the maintenance of genetic diversity. To evaluate this critique, we used the plant-parasitic nematode Meloidogyne arenaria and its natural bacterial parasite Pasteuria penetrans to determine if specificity is altered by temperature. We exposed six isofemale host lines to five parasite sources at three ecologically relevant temperatures. We found that, at two of three temperatures, susceptibility to infection depended on the specific combination of host line and parasite source (G_HxG_P). This specificity varied across temperatures, consistent with a G_HxG_PxE effect. This three-way interaction was driven both by quantitative changes in the strength of specificity across temperatures and shifts in the susceptibility rankings of host-parasite combinations. Our study contributes a rare experimental test of a proposed challenge to the Red Queen Hypothesis and suggests the potential for environmental context to change host-parasite specificity.