THE DYNAMICS OF RECIPROCAL SELECTIVE SWEEPS OF HOST RESISTANCE AND A PARASITE COUNTER-ADAPTATION INDROSOPHILA

Abstract

Host-parasite coevolution can result in consecutive selective sweeps of host resistance alleles and parasite counter-adaptations. To illustrate the dynamics of this important but little studied form of coevolution, we have modeled an ongoing arms race between Drosophila melanogaster and the vertically transmitted sigma virus, using parameters we estimated in the field. We integrate these results with previous work showing that the spread of a resistance allele of the ref(2)P gene in the host was followed by the spread of a virus genotype, which overcomes this resistance. In line with these observations, our model predicts that there can be rapid selective sweeps in both the host and parasite, which can drive large changes in the prevalence of infection. The virus will tend to be ahead in the arms race, as incomplete dominance slows down host adaptation and selection for host resistance is weaker than selection for parasites to overcome resistance-the "life-dinner" principle. This asymmetry in the adaptation rates results in a partial sweep of the host resistance allele, as it loses its advantage part way through the selective sweep. This well-understood natural system illustrates how the outcome of host-parasite coevolution is determined by different population genetic parameters in the field. K E Y W O R D S :Cost of infection, dominance, life dinner principle, partial sweep, speed, selective sweep.

The genetic architecture of resistance to virus infection in Drosophila

“…This is important, as resistance genes may have specific effects on specific virus genotypes, and this may be important in the maintenance of genetic variation and co‐evolution. For example, during the late 20th century genotypes of the sigma virus that were not affected by the resistant allele of ref(2)P spread through European populations of D. melanogaster (Wilfert & Jiggins 2013). Further work could extend this analysis to understand how genetic variation in the virus population interacts with genetic variation in the host population.…”

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

“…Moreover, there is evidence from a range of natural species interactions that is consistent with on-going selective sweeps driven by directional selection (e.g. [28,33–35]). The de-escalatory phase of ERQ dynamics is less well documented, although patterns consistent with ERQ cycles have been described for some of the defensive chemical and counterdefences in wild parsnip and its specialized webworm herbivore [28].…”

Understanding the ecology and evolution of host–parasite interactions across scales

“…). Such asymmetry in adaptation can have important consequences at the population genetic level, for example by hindering selective sweeps of host resistance alleles (Wilfert and Jiggins ). Overall, the population genetic structure of host and parasite populations both shapes and is shaped by migration across an often complex landscape.…”