The geographic structure of pathogen resistance phenotypes under balancing selection

The Red Queen model of host-parasite coevolution is based on time-lagged negative frequency-dependent selection resulting from highly specific interactions of the antagonists within populations. This model has been the preferred theory for explaining the elevated levels of genetic diversity and even trans-species polymorphisms found in the disease genes of many organisms, including humans. Several genomic analyses with plants and animals revealed reduced spatial differentiation and balancing selection at disease genes; however, the geographic distribution of disease-related phenotypes has not been studied. Filling this gap is important, as balancing selection acts on phenotypes, expected to create an even distribution of phenotypes across space. Daphnia magna, a host with strong evidence of Red Queen coevolution, shows a strong pattern of isolation by distance and phylogeographic population structure. Here, we analyse the distribution of resistance phenotypes from 236 populations across 4 continents in response to 14 isolates of the coevolving pathogen Pasteuria ramosa. Polymorphisms for resistance phenotypes show a rather even geographic distribution without isolation by distance and little difference among phylogeographic host clades, coinciding with patterns expected for traits under balancing selection. This finding strongly supports the Red Queen model of antagonistic coevolution by negative frequency-dependent selection. This article is part of the theme issue 'Exploring negative frequency dependent selection across levels: from genetics to ecology and back again'.