Abstract

A priority for biomedical research is to understand the causes of variation in susceptibility to infection. To investigate genetic variation in a model system, we used flies collected from single populations of three different species of Drosophila and artificially selected them for resistance to the parasitoid wasp Leptopilina boulardi, and found that survival rates increased 3 to 30 fold within 6 generations. Resistance in all three species involves a large increase in the number of the circulating hemocytes that kill parasitoids. However, the different species achieve this in different ways, with D. melanogaster moving sessile hemocytes into circulation while the other species simply produce more cells. Therefore, the convergent evolution of the immune phenotype has different developmental bases. These changes are costly, as resistant populations of all three species had greatly reduced larval survival. In all three species resistance is only costly when food is in short supply, and resistance was rapidly lost from D. melanogaster populations when food is restricted. Furthermore, evolving resistance to L. boulardi resulted in cross-resistance against other parasitoids. Therefore, whether a population evolves resistance will depend on ecological conditions including food availability and the presence of different parasite species.

Highlights

  • Considerable genetic variation in susceptibility to infection exists both within and between populations [1]

  • We have found that three species of fruit fly evolve resistance to parasitic wasps by increasing investment in their immune defences but they achieve this in different ways

  • Whether a population evolves resistance depends on ecological conditions, as resistance is only costly when food is in short supply, and evolving resistance to one parasite can have the added benefit of providing resistance to other parasites

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Summary

Introduction

Considerable genetic variation in susceptibility to infection exists both within and between populations [1]. This variation determines the burden of disease within populations, and represents the raw material from which populations can evolve resistance in nature and during the selective breeding of plants and animals. In cases where parasites act as a strong selective pressure on populations, natural selection is expected to eliminate susceptible alleles, reducing genetic variation for resistance [4,5,6,7]. Genetic variation can be maintained if there is a cost to possessing and maintaining the machinery of resistance [8]. Constitutive costs are associated with possessing and maintaining resistance machinery, and are borne even by uninfected individuals [4]

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