Nejvíce citovaný článek - PubMed ID 21104410
Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe
Polymorphism of the major histocompatibility complex (MHC), DAB1 gene was characterized for the first time in the European bitterling (Rhodeus amarus), a freshwater fish employed in studies of host-parasite coevolution and mate choice, taking advantage of newly designed primers coupled with high-throughput amplicon sequencing. Across 221 genotyped individuals, we detected 1-4 variants per fish, with 28% individuals possessing 3-4 variants. We identified 36 DAB1 variants, and they showed high sequence diversity mostly located within predicted antigen-binding sites, and both global and codon-specific excess of non-synonymous mutations. Despite deep divergence between two major allelic lineages, functional diversity was surprisingly low (3 supertypes). Overall, these findings suggest the role of positive and balancing selection in promotion and long-time maintenance of DAB1 polymorphism. Further investigations will clarify the role of pathogen-mediated selection to drive the evolution of DAB1 variation.
- Klíčová slova
- Gene duplication, MHC class IIB, MHC supertypes, Positive selection, Positively selected sites, Rhodeus amarus,
- MeSH
- alely MeSH
- Cyprinidae * genetika parazitologie MeSH
- fylogeneze MeSH
- genetická variace MeSH
- geny MHC třídy II MeSH
- hlavní histokompatibilní komplex MeSH
- molekulární evoluce MeSH
- selekce (genetika) MeSH
- variabilita počtu kopií segmentů DNA * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The genes of the major histocompatibility complex (MHC) are an essential component of the vertebrate immune system and MHC genotypes may determine individual susceptibility to parasite infection. In the wild, selection that favors MHC variability can create situations in which interspecies hybrids experience a survival advantage. In a wild system of two naturally hybridizing leuciscid fish, we assessed MHC IIB genetic variability and its potential relationships to hosts' ectoparasite communities. High proportions of MHC alleles and parasites were species-specific. Strong positive selection at specific MHC codons was detected in both species and hybrids. MHC allele expression in hybrids was slightly biased towards the maternal species. Controlling for a strong seasonal effect on parasite communities, we found no clear associations between host-specific parasites and MHC alleles or MHC supertypes. Hybrids shared more MHC alleles with the more MHC-diverse parental species, but expressed intermediate numbers of MHC alleles and positively selected sites. Hybrids carried significantly fewer ectoparasites than either parent species, suggesting a hybrid advantage via potential heterosis.
- MeSH
- alely * MeSH
- Bayesova věta MeSH
- biologická evoluce * MeSH
- biologické modely MeSH
- Cyprinidae genetika MeSH
- hlavní histokompatibilní komplex MeSH
- hybridizace genetická * MeSH
- hybridní efekt * genetika MeSH
- křížení genetické MeSH
- lineární modely MeSH
- selekce (genetika) * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The genes of major histocompatibility complex (MHC) provide an excellent opportunity to study host-parasite relationships because they are expected to evolve in response to parasites and variation in parasite communities. In this study, we investigated the potential role of parasite-mediated selection acting on MHC class IIB (DAB) genes in European chub (Squalius cephalus) natural populations. We found significant differences between populations in metazoan parasites, neutral and adaptive genetic diversities. The analyses based on pairwise data revealed that populations with dissimilar MHC allelic profiles were geographically distant populations with significantly different diversity in microsatellites and a dissimilar composition of parasite communities. The results from the generalized estimating equations method (GEE) on the level of individuals revealed that metazoan parasite load in European chub was influenced by the diversity of DAB alleles as well as by the diversity of neutral genetic markers and host traits reflecting condition and immunocompetence. The multivariate co-inertia analysis showed specific associations between DAB alleles and parasite species. DAB1-like alleles were more involved in associations with ectoparasites, while DAB3-like alleles were positively associated with endoparasites which could suggest potential differences between DAB genes caused by different selection pressure. Our study revealed that parasite-mediated selection is not the only variable affecting MHC diversity in European chub; however, we strongly support the role of neutral processes as the main driver of DAB diversity across populations. In addition, our study contributes to the understanding of the evolution of MHC genes in wild living fish.
- Klíčová slova
- Genetic diversity, Major histocompatibility complex, Metazoan parasites, Microsatellites, Parasite-driven balancing selection, Phylogeography,
- MeSH
- alely MeSH
- Cyprinidae genetika MeSH
- divoká zvířata MeSH
- genetická variace * MeSH
- hlavní histokompatibilní komplex genetika MeSH
- interakce hostitele a parazita MeSH
- mikrosatelitní repetice genetika MeSH
- nemoci ryb parazitologie MeSH
- parazitární nemoci u zvířat epidemiologie genetika parazitologie MeSH
- paraziti MeSH
- selekce (genetika) * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa epidemiologie MeSH
Two cyprinid species, Parachondrostoma toxostoma, an endemic threatened species, and Chondrostoma nasus, an invasive species, live in sympatry in southern France and form two sympatric zones where the presence of intergeneric hybrids is reported. To estimate the potential threat to endemic species linked to the introduction of invasive species, we focused on the DAB genes (functional MHC IIB genes) because of their adaptive significance and role in parasite resistance. More specifically, we investigated (1) the variability of MHC IIB genes, (2) the selection pattern shaping MHC polymorphism, and (3) the extent to which trans-species evolution and intergeneric hybridization affect MHC polymorphism. In sympatric areas, the native species has more diversified MHC IIB genes when compared to the invasive species, probably resulting from the different origins and dispersal of both species. A similar level of MHC polymorphism was found at population level in both species, suggesting similar mechanisms generating MHC diversity. In contrast, a higher number of DAB-like alleles per specimen were found in invasive species. Invasive species tended to express the alleles of two DAB lineages, whilst native species tended to express the alleles of only the DAB3 lineage. Hybrids have a pattern of MHC expression intermediate between both species. Whilst positive selection acting on peptide binding sites (PBS) was demonstrated in both species, a slightly higher number of positively selected sites were identified in C. nasus, which could result from parasite-mediated selection. Bayesian clustering analysis revealed a similar pattern of structuring for the genetic variation when using microsatellites or the MHC approach. We confirmed the importance of trans-species evolution for MHC polymorphism. In addition, we demonstrated bidirectional gene flow for MHC IIB genes in sympatric areas. The positive significant correlation between MHC and microsatellites suggests that demographic factors may contribute to MHC variation on a short time scale.
- MeSH
- alely MeSH
- Bayesova věta MeSH
- Cyprinidae klasifikace genetika MeSH
- fylogeneze MeSH
- geny MHC třídy II * MeSH
- molekulární evoluce * MeSH
- ohrožené druhy * MeSH
- polymorfismus genetický MeSH
- rekombinace genetická MeSH
- zavlečené druhy MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: The gibel carp is a fish species with dual reproduction modes, gynogenesis and sexual reproduction, coexisting in mixed diploid-polyploid populations. Following the Red Queen (RQ) assumption, asexual organisms are, due to their low genetic diversity, targets for parasite adaptation. Because MHC polymorphism is maintained by selection from parasites and sexual selection, MHC genes are considered as a suitable candidate for testing the RQ hypothesis. In this study, we investigated MHC variability and the selection pressure acting on MHC genes in sexual diploids and asexual triploids. In addition, we tested whether the asexual form of gibel carp suffers from higher parasite loads than the sexual form. RESULTS: At the population level, genotype and allelic diversity of MHC were reduced in gynogenetic triploids when compared to sexual diploids. Different patterns in positively selected sites (PSS) between gynogens and sexual gibel carp were also found. A weak difference in parasite species richness was found between sexual fish and gynogens. However, two common clones of gynogens were significantly more parasitized than sexual diploids or other gynogens with rare MHC genotypes. At the individual level, the higher number of alleles was not associated with higher parasitism in either sexual diploids or gynogens. CONCLUSIONS: The differences in MHC diversity between gynogenetic triploids and sexual diploids are in accordance with the hypothesis of sexually-mediated selection increasing MHC diversity and fulfil a prerequisite of the Red Queen hypothesis. The different patterns in PSS between gynogens and sexual gibel carp also suggest the potential role of sexual selection and supports parasite-mediated selection maintaining MHC diversity. We showed that the most common MHC genotypes of gynogenetic triploids are the target of parasite selection. Our results suggest that the MHC genotype in gibel carp is more important than allelic number for immunocompetence.
- MeSH
- diploidie * MeSH
- genetická variace MeSH
- genotyp MeSH
- hlavní histokompatibilní komplex * MeSH
- kapři genetika fyziologie MeSH
- rozmnožování * MeSH
- rybí proteiny genetika MeSH
- triploidie * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rybí proteiny MeSH