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Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection
Jakob Lohm1, Mats Grahn, Asa Langefors
1Department of Animal Ecology, Ecology Building, Lund University, SE-223 62 Lund, Sweden. jakob.lohm@zooekol.lu.se
Abstract:
The extreme polymorphism found at some major histocompatibility complex (MHC) loci is believed to be maintained by balancing selection caused by infectious pathogens. Experimental support for this is inconclusive. We have studied the interaction between certain MHC alleles and the bacterium Aeromonas salmonicida, which causes the severe disease furunculosis, in Atlantic salmon (Salmo salar L.). We designed full-sibling broods consisting of combinations of homozygote and heterozygote genotypes with respect to resistance or susceptibility alleles. The juveniles were experimentally infected with A. salmonicida and their individual survival was monitored. By comparing full siblings carrying different MHC genotypes the effects on survival due to other segregating genes were minimized. We show that a pathogen has the potential to cause very intense selection pressure on particular MHC alleles; the relative fitness difference between individuals carrying different MHC alleles was as high as 0.5. A co-dominant pattern of disease resistance/susceptibility was found, indicative of qualitative difference in the immune response between individuals carrying the high- and low-resistance alleles. Rather unexpectedly, survival was not higher among heterozygous individuals as compared with homozygous ones.
Insights
Infectious pathogens can drive intense selection on major histocompatibility complex (MHC) alleles in Atlantic salmon. Contrary to expectations, heterozygous individuals did not show increased survival against furunculosis.
Area of Science:
- Immunogenetics
- Evolutionary biology
- Aquaculture
Background:
- The extreme polymorphism in major histocompatibility complex (MHC) genes is hypothesized to be maintained by balancing selection due to infectious diseases.
- Experimental evidence linking specific MHC alleles to pathogen resistance and balancing selection remains inconclusive.
Purpose of the Study:
- To investigate the relationship between specific MHC genotypes and survival in Atlantic salmon experimentally infected with Aeromonas salmonicida.
- To assess the selection pressure exerted by a pathogen on MHC alleles and evaluate the disease resistance patterns.
Main Methods:
- Utilized full-sibling broods of Atlantic salmon with controlled homozygote and heterozygote MHC genotypes.
- Experimentally infected juvenile salmon with Aeromonas salmonicida, monitoring individual survival rates.
- Minimized the influence of other genes by comparing survival within full-sibling groups with differing MHC genotypes.
Main Results:
- Demonstrated that Aeromonas salmonicida can impose intense selection pressure on specific MHC alleles, with fitness differences up to 0.5.
- Observed a co-dominant pattern of disease resistance and susceptibility, suggesting distinct immune responses based on MHC alleles.
- Found no survival advantage for heterozygous individuals compared to homozygous ones, which was an unexpected outcome.
Conclusions:
- Specific MHC alleles are under strong selection pressure from pathogens, supporting the balancing selection hypothesis.
- The interaction between MHC genotype and pathogen resistance is complex, with co-dominance observed in disease response.
- Heterozygote advantage was not detected in this study, challenging a common assumption in MHC-pathogen interaction research.