Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex

Westerdahl, Helena; Asghar, Muhammad; Hasselquist, Dennis; Bensch, Staffan

doi:10.1098/rspb.2011.0917

Cited by 81 publications

(106 citation statements)

References 57 publications

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“…Hence, the findings of this study imply that different Mhc supertypes can confer both qualitative and quantitative resistance to different Plasmodium species in a single host population. Different types of associations between immuno-alleles and the probability of infection are common for different levels of infection severity [21]. Virulent parasites are likely to induce mortality during the acute stage of infection and are difficult to suppress completely [52].…”

Section: Discussionmentioning

confidence: 99%

“…Until recently, positive associations between Mhc alleles and parasite prevalence had been taken as evidence of susceptibility to disease, while the potential for quantitative resistance (immunoalleles that reduce the development of infection) has been largely neglected (see [21]). In this study, we incorporated a detailed investigation of avian malaria infection and analysis of Mhc class I genes in a wild great tit population, to understand the role that Mhc genes play in determining host resistance and susceptibility to Plasmodium infections.…”

Section: Discussionmentioning

confidence: 99%

“…First, as proposed by Westerdahl et al [21], we assessed whether P. circumflexum parasitaemia varied according to the presence of the Mhc supertype, using a linear mixed effects model. Again, if 2 years data were available for an individual, one was randomly excluded from the analysis.…”

Section: (E) Statistical Analysesmentioning

confidence: 99%

“…Total DNA was measured using a Picogreen assay (Quant-iT Picogreen dsDNA assay kit, Invitrogen, Grand Island, NY, USA) and diluted to a concentration of 2 ng ml 21 for Plasmodium quantification [35]. A quantitative-polymerase chain reaction rspb.royalsocietypublishing.org Proc R Soc B 280: 20130134 (qPCR)-based assay was used for measuring parasitaemia.…”

Section: (B) Screening Of Plasmodium Infectionsmentioning

confidence: 99%

“…Alternatively, they may arise as a consequence of quantitative disease-resistance alleles that limit the deleterious effects of disease without eradicating it completely. For example, in great reed warbler (Acrocephalus arundinaceus) populations, a positive relationship between a specific Mhc allele and Plasmodium infection was interpreted as quantitative resistance because parasitaemia ( parasite load) was lower in individuals carrying the allele [21]. Selection might favour such alleles if individuals carrying them were better able to suppress acute infection and hence experienced improved survival relative to those without it, generating a positive relationship between presence of this allele and host infection.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

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Major histocompatibility complex (Mhc) genes are believed to play a key role in the genetic basis of disease control. Although numerous studies have sought links between Mhc and disease prevalence, many have ignored the ecological and epidemiological aspects of the host-parasite interaction. Consequently, interpreting associations between prevalence and Mhc has been difficult, whereas discriminating alleles for qualitative resistance, quantitative resistance and susceptibility remains challenging. Moreover, most studies to date have quantified associations between genotypes and disease status, overlooking the complex relationship between genotype and the properties of the Mhc molecule that interacts with parasites. Here, we address these problems and demonstrate avian malaria (Plasmodium) parasite species-specific associations with functional properties of Mhc molecules (Mhc supertypes) in a wild great tit (Parus major) population. We further show that correctly interpreting these associations depends crucially on understanding the spatial variation in risk of infection and the fitness effects of infection. We report that a single Mhc supertype confers qualitative resistance to Plasmodium relictum, whereas a different Mhc supertype confers quantitative resistance to Plasmodium circumflexum infections. Furthermore, we demonstrate common functional properties of Plasmodium-resistance alleles in passerine birds, suggesting this is a model system for parasite-Mhc associations in the wild.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: (E) Statistical Analysesmentioning

confidence: 99%

Section: (B) Screening Of Plasmodium Infectionsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

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Spatially variable coevolution between a haemosporidian parasite and the MHC of a widely distributed passerine

Jones

Cheviron

Carling

2015

Ecology and Evolution

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The environment shapes host–parasite interactions, but how environmental variation affects the diversity and composition of parasite-defense genes of hosts is unresolved. In vertebrates, the highly variable major histocompatibility complex (MHC) gene family plays an essential role in the adaptive immune system by recognizing pathogen infection and initiating the cellular immune response. Investigating MHC-parasite associations across heterogeneous landscapes may elucidate the role of spatially fluctuating selection in the maintenance of high levels of genetic variation at the MHC. We studied patterns of association between an avian haemosporidian blood parasite and the MHC of rufous-collared sparrows (Zonotrichia capensis) that inhabit environments with widely varying haemosporidian infection prevalence in the Peruvian Andes. MHC diversity peaked in populations with high infection prevalence, although intra-individual MHC diversity was not associated with infection status. MHC nucleotide and protein sequences associated with infection absence tended to be rare, consistent with negative frequency-dependent selection. We found an MHC variant associated with a ∽26% decrease in infection probability at middle elevations (1501–3100 m) where prevalence was highest. Several other variants were associated with a significant increase in infection probability in low haemosporidian prevalence environments, which can be interpreted as susceptibility or quantitative resistance. Our study highlights important challenges in understanding MHC evolution in natural systems, but may point to a role of negative frequency-dependent selection and fluctuating spatial selection in the evolution of Z. capensisMHC.

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Major histocompatibility complex classII DABalleles associated with intestinal parasite load in the vulnerable Chinese egret (Egretta eulophotes)

Wei

Zhou

Fang

et al. 2016

Ecology and Evolution

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The maintenance of major histocompatibility complex (MHC) polymorphism has been hypothesized to result from many mechanisms such as rare‐allele advantage, heterozygote advantage, and allele counting. In the study reported herein, 224 vulnerable Chinese egrets (Egretta eulophotes) were used to examine these hypotheses as empirical results derived from bird studies are rare. Parasite survey showed that 147 (65.63%) individuals were infected with 1–3 helminths, and 82.31% of these infected individuals carried Ascaridia sp. Using asymmetric polymerase chain reaction technique, 10 DAB1, twelve DAB2, and three DAB3 exon 2 alleles were identified at each single locus. A significant association of the rare allele Egeu‐DAB2*05 (allele frequency: 0.022) with helminth resistance was found for all helminths, as well as for the most abundant morphotype Ascaridia sp. in the separate analyses. Egeu‐DAB2*05 occurred frequently in uninfected individuals, and individuals carrying Egeu‐DAB2*05 had significantly lower helminth morphotypes per individual (HMI) (the number of HMI) and the fecal egg count values. Further, the parasite infection measurements were consistently lower in individuals with an intermediate number of different alleles in the duplicated DAB loci. Significantly, heterozygosity within each DAB locus was not correlated with any parasite infection measurements. These results indicate that the diversity in MHC Egeu‐DAB gene is associated with intestinal parasite load and maintained by pathogen‐driven selection that probably operate through both the rare‐allele advantage and the allele counting strategy, and suggest that Egeu‐DAB2*05 might be a valuable indicator of better resistance to helminth diseases in the vulnerable Chinese egret.

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Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex

Cited by 81 publications

References 57 publications

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

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

Spatially variable coevolution between a haemosporidian parasite and the MHC of a widely distributed passerine

Major histocompatibility complex classII DABalleles associated with intestinal parasite load in the vulnerable Chinese egret (Egretta eulophotes)

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