Abstract
The major histocompatibility complex (MHC) plays an important role in infectious disease resistance. The presence of certain MHC alleles and functionally similar groups of MHC alleles (i.e., supertypes) has been associated with resistance to particular parasite species. Farmed and domesticated fish stocks are often depleted in their MHC alleles and supertype diversity, possibly as a consequence of artificial selection for desirable traits, inbreeding (loss of heterozygosity), genetic drift (loss of allelic diversity) and/or reduced parasite biodiversity. Here we quantify the effects of depletion of MHC class II genotype and supertype variation on resistance to the parasite Gyrodactylus turnbulli in guppies (Poecilia reticulata). Compared to the descendants of wild‐caught guppies, ornamental fish had a significantly reduced MHC variation (i.e., the numbers of MHC alleles and supertypes per individual, and per population). In addition, ornamental fish were significantly more susceptible to G. turnbulli infections, accumulating peak intensity 10 times higher than that of their wildtype counterparts. Four out of 13 supertypes were associated with a significantly reduced parasite load, and the presence of some supertypes had a dramatic effect on the intensity of infection. Remarkably, the ornamental and wildtype fish differed in the supertypes that were associated with parasite resistance. Analysis with a genetic algorithm showed that resistance‐conferring supertypes of the wildtype and ornamental fish shared two unique amino acids in the peptide‐binding region of the MHC that were not found in any other alleles. These data show that the supertype demarcation captures some, but not all, of the variation in the immune function of the alleles. This study highlights the importance of managing functional MHC diversity in livestock, and suggests there might be some immunological redundancy among MHC supertypes.
Highlights
The major histocompatibility complex (MHC) is a multigene family that plays an integral part in raising an adaptive immune response that is unique to the jawed vertebrates (Cooper & Alder, 2006)
We assessed the MHC) class II genotypes and immunocompetence of a model fish species, the guppy Poecilia reticulata, comparing recent descendants of wild caught guppies (“wildtype” guppies) with guppies from the pet trade that have been selectively bred over decades (“ornamental” guppies)
The number of MHC alleles and MHC supertypes per individual was significantly lower in ornamental guppies than in wildtype guppies
Summary
The major histocompatibility complex (MHC) is a multigene family that plays an integral part in raising an adaptive immune response that is unique to the jawed vertebrates (Cooper & Alder, 2006). Limited exposure to a range of parasites is likely to weaken the strength of (parasite-mediated) balancing selection, potentially resulting in the loss of immunogenetic polymorphisms This may be critical for genes with exceptionally high levels of polymorphism such as the MHC, which are likely to suffer from the gradual loss of allelic variation and supertype diversity over time, in a phenomenon known as the “drift debt” (Gilroy et al, 2017). Gyrodactylus species are ectoparasites that can be monitored over time in the laboratory, without destructive sampling (Cable, 2011) This makes them exceptional models to study host–parasite dynamics and quantify the impact of potential erosion of MHC supertype variation during domestication. 762 ornamental (from 11 strains) and 294 wildtype (from two rivers) fish were fin clipped for genetic analysis; a subsample of these fish was available for infection studies
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