Dataset Information

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

ABSTRACT: BACKGROUND:The Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates and consists of the most polymorphic genes known to date. Due to this complexity, however, MHC remains to be characterized in many species including any Neotropical cichlid fish. Neotropical crater lake cichlids are ideal models to study evolutionary processes as they display one of the most convincing examples of sympatric and repeated parallel radiation events within and among isolated crater lakes. RESULTS:Here, we characterized the genes of MHC class IIB chain of the Midas cichlid species complex (Amphilophus cf. citrinellus) including fish from five lakes in Nicaragua. We designed 19 new specific primers anchored in a stepwise fashion in order to detect all alleles present. We obtained 866 genomic DNA (gDNA) sequences from thirteen individuals and 756 additional sequences from complementary DNA (cDNA) of seven of those individuals. We identified 69 distinct alleles with up to 25 alleles per individual. We also found considerable intron length variation and mismatches of alleles detected in cDNA and gDNA suggesting that some loci have undergone pseudogenization. Lastly, we created a model of protein structure homology for each allele and identified their key structural components. CONCLUSIONS:Overall, the Midas cichlid has one of the most diverse repertoires of MHC class IIB genes known, which could serve as a powerful tool to elucidate the process of divergent radiations, colonization and speciation in sympatry.

SUBMITTER: Hofmann MJ

PROVIDER: S-EPMC5310070 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

Hofmann Melinda J MJ Bracamonte Seraina E SE Eizaguirre Christophe C Barluenga Marta M

BMC genetics 20170215 1

<h4>Background</h4>The Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates and consists of the most polymorphic genes known to date. Due to this complexity, however, MHC remains to be characterized in many species including any Neotropical cichlid fish. Neotropical crater lake cichlids are ideal models to study evolutionary processes as they display one of the most convincing examples of sympatric and repeated parallel radiation events withi ...[more]

PMID: 28201988

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Project description:IntroductionThe Major Histocompatibility Complex (MHC) of vertebrates is a dynamically evolving multigene family primarily responsible for recognizing non-self peptide antigens and triggering a pathogen-specific adaptive immune response. In birds, the MHC was previously thought to evolve via concerted evolution with high degree of gene homogenization and the rapid loss of orthology. However, the discovery of two ancient avian MHC-IIB gene lineages (DAB1 and DAB2) originating before the radiation of extant birds indicated that despite the action of concerted evolution, orthology may be detectable for long evolutionary periods.MethodsHere, we take advantage of rapidly accumulating digital genomic resources to search for the signal of an ancient duplication at the avian MHC-IIA genes, as well as to compare phylogenetic distribution and selection between MHC-IIA and IIB gene lineages.ResultsThe analysis of MHC sequences from over 230 species representing ca. 70 bird families revealed the presence of two ancient MHC-IIA gene lineages (DAA1 and DAA2) and showed that their phylogenetic distribution matches exactly the distribution of DAB1 and DAB2 lineages, suggesting tight coevolution. The early post-duplication divergence of DAA1 and DAA2 was driven by positive selection fixing radical amino acid differences within the membrane-proximal domain and, most probably, being functionally related to the interactions between α2 and β2 chains of the MHC-II heterodimer. We detected no evidence for an overall (gene-wide) relaxation or intensification of selection at either DAA1/DAB1 or DAA2/DAB2, but codon-specific differences in selection signature were found at the peptide-binding sites between the two gene lineages, perhaps implying specialization to different pathogen regimes.DiscussionOur results suggest that specific pairing of MHC-II α and β chains may have an adaptive significance, a conclusion that advances knowledge on the macroevolution of the avian MHC-II and opens exciting novel directions for future research.

Project description:Host-pathogen interactions are a major evolutionary force promoting local adaptation. Genes of the major histocompatibility complex (MHC) represent unique candidates to investigate evolutionary processes driving local adaptation to parasite communities. The present study aimed at identifying the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of European minnows (Phoxinus phoxinus). To this end, we isolated and genotyped exon 2 of two MHCIIB gene duplicates (DAB1 and DAB3) and 1'665 amplified fragment length polymorphism (AFLP) markers in nine populations, and characterized local bacterial communities by 16S rDNA barcoding using 454 amplicon sequencing. Both MHCIIB loci exhibited signs of historical balancing selection. Whereas genetic differentiation exceeded that of neutral markers at both loci, the populations' genetic diversities were positively correlated with local pathogen diversities only at DAB3. Overall, our results suggest pathogen-mediated local adaptation in European minnows at both MHCIIB loci. While at DAB1 selection appears to favor different alleles among populations, this is only partially the case in DAB3, which appears to be locally adapted to pathogen communities in terms of genetic diversity. These results provide new insights into the importance of host-pathogen interactions in driving local adaptation in the European minnow, and highlight that the importance of adaptive processes driving MHCIIB gene evolution may differ among duplicates within species, presumably as a consequence of alternative selective regimes or different genomic context. Using next-generation sequencing, the present manuscript identifies the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of a cyprinid fish: the European minnow (Phoxinus phoxinus). We highlight that the relative importance of neutral versus adaptive processes in shaping immune competence may differ between duplicates as a consequence of alternative selective regimes or different genomic contexts.

Dataset Information

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

Publications

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

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