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Abstract

Host-pathogen interactions are often characterized by a long-term evolutionary stasis. The Red Queen hypothesis posits that this apparent stability is actually maintained by constant evolution in both species, either through parallel positive selection or fluctuation of alleles under balancing selection. Yet, most described cases of balancing selection are limited to the short term, perhaps because its signature erodes over evolutionary time. We take advantage of the expanded footprint of balancing selection after genetic bottleneck and the transition to self fertilization in the genus Capsella. Contrary to work in other taxa, we document a very uneven reduction in genetic diversity, with ancestral variation persisting preferentially at immunity related loci. Comparisons between anciently diverged lineages reveals the same collection of alleles has been maintained for millions of years. Our results indicate that population longevity in the face of pathogen attack is dependent on the persistence of ancient genetic variation.