Co-adapting but not static predators facilitate prey adaptation to a fluctuating environment

Understanding how ecological interactions among species influence adaptation and population persistence in the face of environmental change is one of the greatest challenges for modern ecology and evolution, with important implications for conservation and other applied fields. As a ubiquitous interaction with potentially strong demographic and selective effects, predation is likely to alter how prey respond to a changing environment. However, whether and how adaptation in prey depends on the way selection operates on predators remains little understood. We investigate this question by combining the theory of adaptive tracking of a moving optimum with trait-matching predator-prey coevolution. We first show that, when coevolutionary processes emerge explicitly from interactions at the individual level, prey maladaptation in any environment does not increase linearly with the difference between the optimum phenotypes for predators and for prey, contrary to the predictions from most earlier coevolutionary models. Furthermore in a fluctuating environment, whether and how the predator evolves crucially affects how well the prey are able to track the moving optimum. Adaptive tracking in prey is facilitated when predators track the same optimum, but hampered when predators are selected towards a fixed optimum. When eco-evolutionary dynamics can occur, phenotypically mismatched predators have a reduced population size that decreases the strength of predatory selection and the intensity of coevolution, but the qualitative influence of predators on prey adaptation remains otherwise similar. Our findings highlight the importance of the evolutionary context of predators for their impacts on prey, and challenge conservation strategies based on predatory attenuation to benefit the prey. Significance statementSpecies in the wild face the dual challenge of adapting to changes in their physical environment and coping with detrimental interactions with other species, such as predators. While evolution by natural selection may jointly overcome both these challenges, the outcome of this process depends on how predator-prey coevolution interacts with environmental adaptation. Here, we show that the influence of coevolving predators on prey adaptation to a changing environment strongly depends on the selective scenario for the predators. Adaptation in prey is facilitated if selective predators also track the changing environment, but hampered if predators are selected towards a constant optimum phenotype, or cannot evolve. Our results challenge the relevance of predator removal as a conservation strategy for prey species.