Many exploited fish species are threatened with collapse and the European eel is no exception. Its abundance has declined dramatically and various reasons account for this, among them the introduction of the invasive swim bladder nematode Anguillicola crassus. For developing an adequate immune response against this parasite, variation at the genes of the major histocompatibility complex (MHC), a key component of the adaptive immune system, might be essential and assessing their diversity might provide critical information for improving conservation strategies. Here, we characterized the MHC class II of the European eel. We provide evidence for relatively high diversity at both MHC IIA and MHC IIB, which contrasts with findings for other endangered species. Furthermore, both genes show signs of site-specific positive selection. The absence of overall positive selection at MHC IIB might, however, suggests that demographic shifts have negatively impacted that gene, thereby possibly reducing the adaptive potential of the European eel.

Invasive parasites are involved in population declines of new host species worldwide. The high susceptibilities observed in many novel hosts have been attributed to the lack of protective immunity to the parasites which native hosts acquired during their shared evolution. We experimentally infected Japanese eels (Anguilla japonica) and European eels (Anguilla anguilla) with Anguillicola crassus, a nematode parasite that is native to the Japanese eel and invasive in the European eel. We inferred gene expression changes in head kidney tissue from both species, using RNA‐seq data to determine the responses at two time points during the early stages of infection (3 and 23 days postinfection). At both time points, the novel host modified the expression of a larger and functionally more diverse set of genes than the native host. Strikingly, the native host regulated immune gene expression only at the earlier time point and to a small extent while the novel host regulated these genes at both time points. A low number of differentially expressed immune genes, especially in the native host, suggest that a systemic immune response was of minor importance during the early stages of infection. Transcript abundance of genes involved in cell respiration was reduced in the novel host which may affect its ability to cope with harsh conditions and energetically demanding activities. The observed gene expression changes in response to a novel parasite that we observed in a fish follow a general pattern observed in amphibians and mammals, and suggest that the disruption of physiological processes, rather than the absence of an immediate immune response, is responsible for the higher susceptibility of the novel host.

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BackgroundThe 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.ResultsHere, 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.ConclusionsOverall, 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12863-017-0474-x) contains supplementary material, which is available to authorized users.

Background Ecological diversification is the result of divergent natural selection by contrasting habitat characteristics that favours the evolution of distinct phenotypes. This process can happen in sympatry and in allopatry. Habitat-specific parasite communities have the potential to drive diversification among host populations by imposing selective pressures on their host's immune system. In particular, the hyperdiverse genes of the major histocompatibility complex (MHC) are implicated in parasite-mediated host divergence. Here, we studied the extent of divergence at MHC, and discuss how it may have contributed to the Nicaraguan Midas cichlid species complex diversification, one of the most convincing examples of rapid sympatric parallel speciation. Results We genotyped the MHC IIB for individuals from six sympatric Midas cichlid assemblages, each containing species that have adapted to exploit similar habitats. We recovered large allelic and functional diversity within the species complex. While most alleles were rare, functional groups of alleles (supertypes) were common, suggesting that they are key to survival and that they were maintained during colonization and subsequent radiations. We identified lake-specific and habitat-specific signatures for both allelic and functional diversity, but no clear pattern of parallel divergence among ecomorphologically similar phenotypes. Conclusions Colonization and demographic effects of the fish could have contributed to MHC evolution in the Midas cichlid in conjunction with habitat-specific selective pressures, such as parasites associated to alternative preys or environmental features. Additional ecological data will help evaluating the role of host–parasite interactions in the Midas cichlid radiations and aid in elucidating the potential role of non-parallel features differentiating crater lake species assemblages.

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Encapsulation of the parasitic nematode Anguillicola crassus Kuwahara, Niimi & Hagaki is commonly observed in its native host, the Japanese eel (Anguilla japonica Temminck & Schlegel). Encapsulation has also been described in a novel host, the European eel (A. anguilla L.), and there is evidence that encapsulation frequency has increased since the introduction of A. crassus. We examined whether encapsulation of A. crassus provides an advantage to its novel host in Lake Müggelsee, NE Germany. We provide the first evidence that encapsulation was associated with reduced abundance of adult A. crassus. This pattern was consistent in samples taken 3 months apart. There was no influence of infection on the expression of the two metabolic genes studied, but the number of capsules was negatively correlated with the expression of two mhc II genes of the adaptive immune response, suggesting a reduced activation. Interestingly, eels that encapsulated A. crassus had higher abundances of two native parasites compared with non‐encapsulating eels. We propose that the response of A. anguilla to infection by A. crassus may interfere with its reaction to other co‐occurring parasites.

The genes of the major histocompatibility complex (MHC) are among the most polymorphic genes in vertebrates, and crucial for their adaptive immune response. These genes frequently show inconsistencies between allelic genealogies and species phylogenies. This phenomenon is thought to be the result of parasite-mediated balancing selection maintaining ancient alleles through speciation events (trans-species polymorphism, TSP). However, allele similarities may also arise from post-speciation mechanisms, such as convergence or introgression. Here, we investigated the evolution of MHC class IIB diversity in the cichlid fish radiations across Africa and the Neotropics by a comprehensive review of available MHC IIB DNA sequence information. We explored what mechanism explains the MHC allele similarities found among cichlid radiations. Our results showed extensive allele similarity among cichlid fish across continents, likely due to TSP. Functionality at MHC was also shared among species of the different continents. The maintenance of MHC alleles for long evolutionary times and their shared functionality may imply that certain MHC variants are essential in immune adaptation, even in species that diverged millions of years ago and occupy different environments.