Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance

Abstract

Summary 1. An emerging framework in animal disease ecology seeks to ‘decompose’ a host’s response to disease into resistance, or its ability to resist infection following exposure, and tolerance, or its ability to limit the damage associated with infection. How these processes vary over the life history of a host, however, and whether developmental changes in resistance and tolerance account for ‘critical windows’ of disease vulnerability remain open questions. 2. Critical developmental windows are particularly important for infections that alter host development. Recently, increased observations of amphibians with severe limb malformations have stimulated debate over the causes responsible and whether malformation types can be used to infer the agent responsible. The trematode parasite Ribeiroia ondatrae, for example, is often implicated in accounts of extra-legged frogs, but is believed to be unimportant in explaining missing legged animals. Here, we test the influence of host developmental stage, from eggs to post-metamorphosis, on the risk of mortality and the types of malformations produced in Pacific chorus frogs (Pseudacris regilla) following exposure to trematode infection. 3. Consistent with a critical window of vulnerability, host mortality and malformations were greatest among animals exposed during pre-limb and early limb development (15–90%) and decreased to <5% with progressive development. Early stage animals also exhibited a higher frequency of missing limbs, whereas extra limbs and limb elements developed predominantly among tadpoles exposed after limb development was initiated. Hosts infected later in limb development were normal or exhibited only minor outgrowths and abnormal skin webbings. 4. Increases in host tolerance rather than host resistance largely explained the observed changes in pathology. Prior to host metamorphosis, parasites exhibited comparable success invading host tissue, but the amount of resulting damage differed significantly as a function of host size and developmental stage. Following metamorphosis hosts were significantly more resistant to infections, however. 5. These findings highlight the importance of critical developmental windows for infectious diseases and underscore the role of developmental changes in host tolerance in controlling this process. Forecasted changes in climate, for example, have enormous potential to influence both the timing and intensity of host–parasite interactions in nature.