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

Abstract Understanding how ecological interactions among species influence adaptation and population persistence in the face of environmental change is one of the greatest challenges of modern ecology and evolution, with important implications for conservation and other applied fields. Predation being a ubiquitous interaction with potentially strong demographic and selective effects, it 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 here 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 scaling up individual-level processes to the population level, prey maladaptation in any environment is non-linear with respect to the divergence between the prey’s and predator’s optimum, contrary to the predictions from most earlier coevolutionary models. In a fluctuating environment, the influence of a selective predator on tracking of the moving optimum by the prey crucially depends on whether and how the predator itself evolves. In particular, a predator that tracks the same optimum facilitates adaptive tracking in prey, while a predator selected towards a fixed optimum hampers it. When eco-evolutionary dynamics are also allowed, the reduced population size of phenotypically mismatched predators 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. Significance statement Species 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 can potentially overcome both these challenges and rescue populations from extinction, this process can be complicated by interactions between predator-prey coevolution and environmental adaptation. Here, we show that the influence of predators on prey adaptation to a changing environment strongly depends on the selective scenario for the predators: adaptation in prey is facilitated if predators also need to adapt to the changing environment, but hampered if predators are either constant, or selected to be. Our results question conservation strategies based on removing predators to the benefit of prey. Competing Interest Statement The authors have declared no competing interest. Footnotes Competing Interest Statement: No competing interests