The age and evolution of an antiviral resistance mutation in Drosophila melanogaster

Abstract

What selective processes underlie the evolution of parasites and their hosts? Arms-race models propose that new host-resistance mutations or parasite counter-adaptations arise and sweep to fixation. Frequency-dependent models propose that selection favours pathogens adapted to the most common host genotypes, conferring an advantage to rare host genotypes. Distinguishing between these models is empirically difficult. The maintenance of disease-resistance polymorphisms has been studied in detail in plants, but less so in animals, and rarely in natural populations. We have made a detailed study of genetic variation in host resistance in a natural animal population, Drosophila melanogaster, and its natural pathogen, the sigma virus. We confirm previous findings that a single (albeit complex) mutation in the gene ref(2)P confers resistance against sigma and show that this mutation has increased in frequency under positive selection. Previous studies suggested that ref(2)P polymorphism reflects the progress of a very recent selective sweep, and that in Europe during the 1980s, this was followed by a sweep of a sigma virus strain able to infect flies carrying this mutation. We find that the ref(2)P resistance mutation is considerably older than the recent spread of this viral strain and suggest that--possibly because it is recessive--the initial spread of the resistance mutation was very slow.

Figure 1

Mean proportion of individuals infected with the sigma virus. Males and females hemizygous for the ref(2)P gene (encoding the resistant form, Gly; or the susceptible form, Asn–Gln), and males and females heterozygous for the ref(2)P gene (encoding the resistant form, Gly; or the susceptible form, Asn–Gln) are shown.