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The major histocompatibility complex (MHC) is a multigene family responsible for pathogen detection, and initiation of adaptive immune responses. Duplication, natural selection, recombination, and their resulting high functional genetic diversity spread across several duplicated loci are the main hallmarks of the MHC. Although these features were described in several jawed vertebrate lineages, a detailed MHC IIβ characterization at the population level is still lacking for chondrichthyans (chimaeras, rays and sharks), i.e. the most basal lineage to possess an MHC-based adaptive immune system. We used the small-spotted catshark (Scyliorhinus canicula, Carcharhiniformes) as a case-study species to characterize MHC IIβ diversity using complementary molecular tools, including publicly available genome and transcriptome datasets, and a newly developed high-throughput Illumina sequencing protocol. We identified three MHC IIβ loci within the same genomic region, all of which are expressed in different tissues. Genetic screening of the exon 2 in 41 individuals of S. canicula from a single population revealed high levels of sequence diversity, evidence for positive selection, and footprints of recombination. Moreover, the results also suggest the presence of copy number variation in MHC IIβ genes. Thus, the small-spotted catshark exhibits characteristics of functional MHC IIβ genes typically observed in other jawed vertebrates.
The major histocompatibility complex (MHC) is a multigene family responsible for pathogen detection, and initiation of adaptive immune responses. Duplication, natural selection, recombination, and their resulting high functional genetic diversity spread across several duplicated loci are the main hallmarks of the MHC. Although these features were described in several jawed vertebrate lineages, a detailed MHC IIβ characterization at the population level is still lacking for chondrichthyans (chimaeras, rays and sharks), i.e. the most basal lineage to possess an MHC-based adaptive immune system. We used the small-spotted catshark (Scyliorhinus canicula, Carcharhiniformes) as a case-study species to characterize MHC IIβ diversity using complementary molecular tools, including publicly available genome and transcriptome datasets, and a newly developed high-throughput Illumina sequencing protocol. We identified three MHC IIβ loci within the same genomic region, all of which are expressed in different tissues. Genetic screening of the exon 2 in 41 individuals of S. canicula from a single population revealed high levels of sequence diversity, evidence for positive selection, and footprints of recombination. Moreover, the results also suggest the presence of copy number variation in MHC IIβ genes. Thus, the small-spotted catshark exhibits characteristics of functional MHC IIβ genes typically observed in other jawed vertebrates.
The major histocompatibility complex (MHC) has been intensively studied for the relative effects of different evolutionary forces in recent decades. Pathogen-mediated balancing selection is generally thought to explain the high polymorphism observed in MHC genes, but it is still unclear to what extent MHC diversity is shaped by selection relative to neutral drift. In this study, we genotyped MHC class II DRB genes and 15 neutral microsatellite loci across 26 geographic populations of European badgers (Meles meles) covering most of their geographic range. By comparing variation of microsatellite and diversity of MHC at different levels, we demonstrate that both balancing selection and drift have shaped the evolution of MHC genes. When only MHC allelic identity was investigated, the spatial pattern of MHC variation was similar to that of microsatellites. By contrast, when functional aspects of the MHC diversity (e.g., immunological supertypes) were considered, balancing selection appears to decrease genetic structuring across populations. Our comprehensive sampling and analytical approach enable us to conclude that the likely mechanisms of selection are heterozygote advantage and/or rare-allele advantage. This study is a clear demonstration of how both balancing selection and genetic drift simultaneously affect the evolution of MHC genes in a widely distributed wild mammal.
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