A power–efficiency trade‐off in resource use alters epidemiological relationships

Abstract

Trade-offs play pivotal roles in the ecology and evolution of natural populations. However, trade-offs are probably not static, invariant relationships. Instead, ecological factors can shift, alter, or reverse the relationships underlying trade-offs and create critical genotype x environment (G x E) interactions. But which ecological factors alter trade-offs or create G x E interactions, and why (mechanistically) do they do this? We tackle these questions using resource quality as the central ecological factor and a case study of disease in the plankton. We show that clonal genotypes of a zooplankton host (Daphnia dentifera) exhibit a "power-efficiency" trade-off in resource use, where powerful (fast-feeding) host clones perform well on richer algal resources, but more efficient (slow-feeding) clones perform relatively well on poorer resources. This resource-based trade-off then influences epidemiological relationships due to fundamental connections between resources and fecundity, transmission rate (an index of resistance), and replication of a virulent fungal parasite (Metschnikowia bicuspidata) within hosts. For instance, using experiments and dynamic energy budget models, we show that the power-efficiency trade-off overturned a previously detected trade-off between fecundity and transmission risk of hosts to this parasite. When poorer resources were eaten, transmission risk and fecundity were negatively, not positively, correlated. Additionally, poor resource quality changed positive relationships between yield of infectious stages (spores) and host fecundity: those fecundity-spore relationships with poor food became negative or nonsignificant. Finally, the power-efficiency trade-off set up an interaction between host clone and resource quality for yield of fungal spores: powerful clones yielded relatively more spores on the better resource, while efficient clones yielded relatively more on the poorer resource. Thus, the physiological ecology of resource use can offer potent, mechanistic insight linking environmental factors to epidemiological relationships.