Plasmodium relictuminfection 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.

Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population

“…Although population-specific associations between Mhc alleles and Plasmodium species have been reported in house sparrow populations [17,19], the functional differences between these alleles were not assessed, and our results imply that different alleles linked with disease may be similar at their ABS even in unrelated host species. The functional similarity across species suggests that Mhc-linked malaria resistance can be a valuable area for further research to understand the genetic basis of variation in infection in wild systems.…”

“…Of five studies investigating a link between passerine Mhc class I and Plasmodium infection, only two studies, both on house sparrows (Passer domesticus), presented sequence information for Mhc alleles identified as being linked to P. relictum infection (GenBank nos EU715815 -EU715817 and EF429132; [18,19]). The similarity of these house sparrow alleles to the Mhc supertypes examined in this study at their putative ABS (to infer functional similarity) was assessed by combining these additional four alleles with our 755 functional class I alleles and re-running the k-means clustering algorithm [41].…”

“…Alleles that are negatively correlated with host infection are easily interpreted as disease-resistance alleles that provide qualitative protection against the parasite [17,19]. Positive correlations between Mhc alleles and host infection are more difficult to explain, because selection against susceptibility alleles should eliminate them from populations.…”

Host compatibility rather than vector–host-encounter rate determines the host range of avian Plasmodium parasites

“…Alternatively, these hosts may be resistant to the infection. This could be owing to adaptations of the immune system (such as those associated with major histocompatibility complex [62][63][64] or host cell surface proteins [65]), the lack of necessary machinery of the parasite to invade and persist in certain hosts, or both. Palinauskas et al [7] demonstrated that experimentally challenged host species differed in their level of resistance towards Plasmodium relictum.…”

MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus

“…The second mechanism, rare-allele advantage, assumes that parasites are most likely to adapt to the most frequent host genotypes, and thus rare alleles are more often associated with parasite resistance (Bodmer 1972;Potts and Wakeland 1990;Borghans et al 2004). If the selective pressure from a parasite changes temporally (Hill et al 1991) or spatially (Kloch et al 2010;Loiseau et al 2011), this change may drive the third mechanism, fluctuating selection (Hedrick 2002).…”