Sex and the Red Queen

Abstract

Negative frequency-dependent selection exerted by parasites and pathogens can generate a selective advantage for rare host genotypes. This mechanism, known as the Red Queen, is currently considered to be one of the most likely explanations for the predominance of sexual reproduction in natural populations. Even so, the extent to which the Red Queen can and does provide an advantage to sex in nature is fiercely debated. Here, we survey the history of the development of the Red Queen hypothesis as applied to the maintenance of sex and discuss its theoretical underpinnings. We then review and synthesize the current body of theory and empirical data relevant to assessing whether Red Queen dynamics are likely to contribute to any general explanation for why sex is so common. We conclude that while there are many independent lines of evidence in support of a role for the Red Queen, important theoretical and empirical gaps remain. In particular, there is a need for theory addressing the breadth of conditions under which the Red Queen can favor sex, predictions for the patterns of molecular evolution expected for loci under negative frequency-dependent selection, and empirical research evaluating the strength of parasite-mediated selection in nature and the genetics of susceptibility and infection.