Running with the Red Queen: the role of biotic conflicts in evolution

Abstract

What are the causes of natural selection? Over 40 years ago, Van Valen proposed the Red Queen hypothesis, which emphasized the primacy of biotic conflict over abiotic forces in driving selection. Species must continually evolve to survive in the face of their evolving enemies, yet on average their fitness remains unchanged. We define three modes of Red Queen coevolution to unify both fluctuating and directional selection within the Red Queen framework. Empirical evidence from natural interspecific antagonisms provides support for each of these modes of coevolution and suggests that they often operate simultaneously. We argue that understanding the evolutionary forces associated with interspecific interactions requires incorporation of a community framework, in which new interactions occur frequently. During their early phases, these newly established interactions are likely to drive fast evolution of both parties. We further argue that a more complete synthesis of Red Queen forces requires incorporation of the evolutionary conflicts within species that arise from sexual reproduction. Reciprocally, taking the Red Queen's perspective advances our understanding of the evolution of these intraspecific conflicts.

Keywords: Red Queen hypothesis; coevolution; sexual selection.

Figure 1.

Natural systems used to explore Red Queen dynamics. (a–c) FRQ dynamics: (a) stickleback fish and trematode parasites, (b) Potamopyrgus antipodarum snails and trematode parasites, and (c) Daphnia waterfleas and microparasites. (d) Mixed FRQ/ERQ dynamics: Linum marginale and Melampsora rust fungus. (e–g) ERQ dynamics: (e) Taricha newts and Thamnophis snake predators, (f) wild parsnip and predatory webworms, and (g) Camellia and weevil predators. (h) CRQ dynamics: Crossbills and lodgepole pine trees. Photo credits: (a) M. Milinski; (b) C. Lively and G. Harp; (c) J. Wolinska and P. Juracka; (d) P. Thrall and J. Burdon; (e) B. Brodie III; (f) M. Berenbaum; (g) H. Toju; (h) C. Benkman. (Online version in colour.)