Evolution of parasites in the Anthropocene: new pressures, new adaptive directions

The Anthropocene is seeing the human footprint rapidly spreading to all of Earth's ecosystems. The fast-changing biotic and abiotic conditions experienced by all organisms are exerting new and strong selective pressures, and there is a growing list of examples of human-induced evolution in response to anthropogenic impacts. No organism is exempt from these novel selective pressures. Here, we synthesise current knowledge on human-induced evolution in eukaryotic parasites of animals, and present a multidisciplinary framework for its study and monitoring. Parasites generally have short generation times and huge fecundity, features that predispose them for rapid evolution. We begin by reviewing evidence that parasites often have substantial standing genetic variation, and examples of their rapid evolution both under conditions of livestock production and in serial passage experiments. We then present a two-step conceptual overview of the causal chain linking anthropogenic impacts to parasite evolution. First, we review the major anthropogenic factors impacting parasites, and identify the selective pressures they exert on parasites through increased mortality of either infective stages or adult parasites, or through changes in host density, quality or immunity. Second, we discuss what new phenotypic traits are likely to be favoured by the new selective pressures resulting from altered parasite mortality or host changes; we focus mostly on parasite virulence and basic life-history traits, as these most directly influence the transmission success of parasites and the pathology they induce. To illustrate the kinds of evolutionary changes in parasites anticipated in the Anthropocene, we present a few scenarios, either already documented or hypothetical but plausible, involving parasite taxa in livestock, aquaculture and natural systems. Finally, we offer several approaches for investigations and real-time monitoring of rapid, human-induced evolution in parasites, ranging from controlled experiments to the use of state-of-the-art genomic tools. The implications of fast-evolving parasites in the Anthropocene for disease emergence and the dynamics of infections in domestic animals and wildlife are concerning. Broader recognition that it is not only the conditions for parasite transmission that are changing, but the parasites themselves, is needed to meet better the challenges ahead.