Host-pathogen coevolution increases genetic variation in susceptibility to infection

Abstract

35It is common to find considerable genetic variation in susceptibility to infection in natural 36 populations. We have investigated whether natural selection increases this variation by 37 testing whether host populations show more genetic variation in susceptibility to pathogens 38 that they naturally encounter than novel pathogens. In a large cross-infection experiment 39 involving four species of Drosophila and four host-specific viruses, we always found greater 40 genetic variation in susceptibility to viruses that had coevolved with their host. We went on 41 to examine the genetic architecture of resistance in one host species, finding that there are 42 more major-effect genetic variants in coevolved host-parasite interactions. We conclude 43 that selection by pathogens increases genetic variation in host susceptibility, and much of 44 this effect is caused by the occurrence of major-effect resistance polymorphisms within 45 populations.46 47 53 to infection. Insect populations, like those of other organisms, typically contain considerable 54 genetic variation in susceptibility to infection [2, 4, 9, 10], and provide a convenient 55 laboratory model in which to investigate basic questions about how this variation is 56 maintained [11]. Within vector species like mosquitoes, resistant genotypes are less likely to 57 transmit parasites, and this has the potential to reduce disease in vertebrate populations 58 [12]. Where pathogens are contributing the decline of beneficial species like pollinators, high 59 levels of genetic variation may allow populations to recover [13]. Understanding the origins 60 of genetic variation in susceptibility is therefore a fundamental question in infectious disease 61 biology. 63As pathogens are harmful, natural selection is expected to favour resistant host genotypes. 64Directional selection on standing genetic variation will drive alleles to fixation, removing 65 variants from the population [14-16]. However, as directional selection also increases the 66 frequency of mutations that change the trait in the direction of selection, at equilibrium it is 67 expected to have no effect on levels of standing genetic variation (relative to mutation-drift 68 balance; [17]). However, selection mediated by pathogens may be different. Coevolution 69 with pathogens can result in the maintenance of both resistant and susceptible alleles by 70 negative frequency dependent selection [18, 19]. Similarly, when infection prevalence 71 exhibits geographical or temporal variation, selection can maintain genetic variation,72 especially if pleiotropic costs to resistance provide an advantage to susceptible individuals 73 when infection is rare [20-22]. Even when there is simple directional selection on alleles that 74 increase resistance, the direction of selection by pathogens may frequently change so 75 populations may not be at equilibrium. If selection favours rare alleles -such as new 76 mutations -directional selection can transiently increase genetic variation during their 77 spread through t...

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The genetics of exapted resistance to two exotic pathogens in pedunculate oak

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