Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids

Hofmann, Melinda J.; Bracamonte, Seraina E.; Eizaguirre, Christophe; Barluenga, Marta

doi:10.1186/s12863-017-0474-x

Cited by 16 publications

(15 citation statements)

References 98 publications

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“…Due to the extreme polymorphism of MHC genes, especially in cichlids (Klein et al, 1993; Figueroa et al, 2000; Blais et al, 2007; Hofmann et al, 2017), it is notoriously difficult to obtain primers that can amplify all MHC loci within a single species, and presumably impossible to obtain primers that amplify all MHC loci across a wide range of species like the ones in this study. For this reason, we opted to use primers that amplify a subset of MHC loci in all species that we sampled, allowing our results to be comparable across species despite not amplifying the full diversity of MHC.…”

Section: Methodsmentioning

confidence: 93%

“…In teleost fishes, the class II a genes are more conserved than the class II b genes. In cichlids, both groups of genes have oftentimes undergone several duplication events (Sato et al, 2012; Hablützel et al, 2013; Hofmann et al, 2017). MHC evolution is typically characterized by high standing variation (Sommer, 2005), positive and balancing selection (Hughes & Nei, 1988, 1989; Bernatchez & Landry, 2003), gene duplication and loss (Málaga-Trillo et al, 1998; Nei & Rooney, 2005), and extensive trans-species polymorphism (Klein et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…At the intra-specific level, such differentiation has also been described between allopatric populations, suggesting that parasites may represent a divergent selective force promoting divergence in allopatry (Raeymaekers et al, 2013; Grégoir et al, 2015; Hablützel et al, 2016). Second, extensive diversity and variation in MHC gene pools has been observed among cichlid species and populations (Klein et al, 1993; Ono et al, 1993; Málaga-Trillo et al, 1998; Blais et al, 2007; Sato et al, 2012; Hablützel et al, 2013, 2016; Hofmann et al, 2017). Dissimilarities in parasite community composition concur with differentiation of MHC class II genes in closely related cichlid species living in sympatry (Blais et al, 2007), as well as in allopatric populations within species (Hablützel et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation

et al. 2018

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Differences in habitat and diet between species are often associated with morphological differences. Habitat and trophic adaptation have therefore been proposed as important drivers of speciation and adaptive radiation. Importantly, habitat and diet shifts likely impose changes in exposure to different parasites and infection risk. As strong selective agents influencing survival and mate choice, parasites might play an important role in host diversification. We explore this possibility for the adaptive radiation of Lake Tanganyika (LT) cichlids. We first compare metazoan macroparasites infection levels between cichlid tribes. We then describe the cichlids’ genetic diversity at the major histocompatibility complex (MHC), which plays a key role in vertebrate immunity. Finally, we evaluate to what extent trophic ecology and morphology explain variation in infection levels and MHC, accounting for phylogenetic relationships. We show that different cichlid tribes in LT feature partially non-overlapping parasite communities and partially non-overlapping MHC diversity. While morphology explained 15% of the variation in mean parasite abundance, trophic ecology accounted for 16% and 22% of the MHC variation at the nucleotide and at the amino acid level, respectively. Parasitism and immunogenetic adaptation may thus add additional dimensions to the LT cichlid radiation. Electronic supplementary material The online version of this article (10.1007/s10750-018-3798-2) contains supplementary material, which is available to authorized users.

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Section: Methodsmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation

et al. 2018

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“…MHC II molecules are expressed on antigen presenting cells which have direct functional relevance to teleost immune responses ( Janeway et al 2004 ; Chen et al. 2006 ; Hofmann et al. 2017 ) and have been identified in various teleost species ( Grimholt et al.…”

Section: Discussionmentioning

confidence: 99%

“…2000 ; Pang et al. 2013 ; Hofmann et al. 2017 ) with very high allelic diversity maintained by natural and sexual selection ( Aguilar and Garza 2007 ; Consuegra and Garcia de Leaniz 2008 ), which could result in allele specific differences in gene expression.…”

Section: Discussionmentioning

confidence: 99%

Immune-Related Transcriptional Responses to Parasitic Infection in a Naturally Inbred Fish: Roles of Genotype and Individual Variation

Pawluk

Webster

Cable

et al. 2018

Genome Biology and Evolution

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Parasites are strong drivers of evolutionary change and the genetic variation of both host and parasite populations can co-evolve as a function of parasite virulence and host resistance. The role of transcriptome variation in specific interactions between host and parasite genotypes has been less studied and can be confounded by differences in genetic variation. We employed two naturally inbred lines of a self-fertilizing fish to estimate the role of host genotype in the transcriptome response to parasite infection using RNA-seq. In addition, we targeted several differentially expressed immune-related genes to further investigate the relative role of individual variation in the immune response using RT-qPCR, taking advantage of the genomic uniformity of the self-fertilizing lines. We found significant differences in gene expression between lines in response to infection both in the transcriptome and in individual gene RT-qPCR analyses. Individual RT-qPCR analyses of gene expression identified significant variance differences between lines for six genes but only for three genes between infected and control fish. Our results indicate that although the genetic background plays an important role in the transcriptome response to parasites, it cannot fully explain individual differences within genetically homogeneous lines, which can be important for determining the response to parasites.

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Trans‐specific polymorphism and the convergent evolution of supertypes in major histocompatibility complex class II genes in darters (Etheostoma)

Million

Lively

2022

Ecology and Evolution

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Major Histocompatibility Complex (MHC) genes are one of the most polymorphic gene groups known in vertebrates. MHC genes also exhibit allelic variants that are shared among taxa, referred to as trans‐specific polymorphism (TSP). The role that selection plays in maintaining such high diversity within species, as well as TSP, is an ongoing discussion in biology. In this study, we used deep‐sequencing techniques to characterize MHC class IIb gene diversity in three sympatric species of darters. We found at least 5 copies of the MHC gene in darters, with 126 genetic variants encoding 122 unique amino acid sequences. We identified four supertypes based on the binding properties of proteins encoded by the sequences. Although each species had a unique pool of variants, many variants were shared between species pairs and across all three species. Phylogenetic analysis showed that the variants did not group together monophyletically based on species identity or on supertype. An expanded phylogenetic analysis showed that some darter alleles grouped together with alleles from other percid fishes. Our findings show that TSP occurs in darters, which suggests that balancing selection is acting at the genotype level. Supertypes, however, are most likely evolving convergently, as evidenced by the fact that alleles do not form monophyletic groups based on supertype. Our research demonstrates that selection may be acting differently on MHC genes at the genotype and supertype levels, selecting for the maintenance of high genotypic diversity while driving the convergent evolution of similar MHC phenotypes across different species.

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Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids

Cited by 16 publications

References 98 publications

An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation

An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation

Immune-Related Transcriptional Responses to Parasitic Infection in a Naturally Inbred Fish: Roles of Genotype and Individual Variation

Trans‐specific polymorphism and the convergent evolution of supertypes in major histocompatibility complex class II genes in darters (Etheostoma)

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