Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus)

Abstract

Antagonistic coevolution between hosts and parasites has been proposed as a mechanism maintaining genetic diversity in both host and parasite populations. In particular, the high level of genetic diversity usually observed at the major histocompatibility complex (MHC) is generally thought to be maintained by parasite-driven selection. Among the possible ways through which parasites can maintain MHC diversity, diversifying selection has received relatively less attention. This hypothesis is based on the idea that parasites exert spatially variable selection pressures because of heterogeneity in parasite genetic structure, abundance or virulence. Variable selection pressures should select for different host allelic lineages resulting in population-specific associations between MHC alleles and risk of infection. In this study, we took advantage of a large survey of avian malaria in 13 populations of the house sparrow (Passer domesticus) to test this hypothesis. We found that (i) several MHC alleles were either associated with increased or decreased risk to be infected with Plasmodium relictum, (ii) the effects were population specific, and (iii) some alleles had antagonistic effects across populations. Overall, these results support the hypothesis that diversifying selection in space can maintain MHC variation and suggest a pattern of local adaptation where MHC alleles are selected at the local host population level.

Figure 1.

Geographical localization of the 13 house sparrow populations used in this study. Scale bar, 100 km.

Figure 2.

Difference between the percentage of infected individuals carrying the MHC allele and the percentage of infected individuals not carrying the allele, for the five and 10 populations of house sparrows (Passer domesticus) which, respectively, harbour pado83 and pado133. Positive values represent increased risk of infection linked to the presence of the MHC allele, whereas negative values indicate decreased risk associated with the allele. Stars indicate significant association between MHC allele and infection status.