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The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen‐mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC‐DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human‐mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance., We investigate evolutionary mechanisms shaping genetic structure and diversity at the major histocompatibility complex class II gene (MHC‐DAB) in wild populations of Mediterranean brown trout (Salmo trutta L. complex) exposed to introgression from domestic (hatchery) lineages. We reveal the role of historical positive selection and current balancing selection (rare‐allele advantage, but not heterozygote advantage or divergent allele advantage) to mantaining high MHC (functional) polymorhism. Also, we provide evidence for the interplay between genetic drift and human‐mediated introgression to shape MHC diversity and population structure.

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.

Proteins encoded by extraordinarily polymorphic major histocompatibility complex (MHC) genes are involved in the adaptive immune response. Balancing selection is believed to maintain MHC polymorphism in the long term, although neutral processes also play a role in shaping MHC diversity. However, the relative contribution of these processes is poorly understood. Here we characterized MHC class II variation of a low-dispersal, pond-breeding newt (Triturus carnifex) over a restricted, geographically structured area. We aimed to (1) evaluate the contribution of selection and neutral processes to shaping MHC diversity at two geographic scales, and (2) test for signatures of divergent allele advantage (DAA), which is a potentially important mechanism of balancing selection. The dominant role of selection in shaping MHC variation was suggested by the lack of correlation between MHC and neutral (microsatellite) variation. Although most variation occurred within populations for both types of markers, they differed in the extent of structuring at the two spatial scales. MHC structuring was more pronounced at local scales, suggesting the role of local selection, while structuring was not detectable at a larger scale, possibly due to the effect of balancing selection. Microsatellites showed the opposite pattern. As expected under DAA, the observed genotypes combined more sequence diversity than expected under a random association of alleles. Thus, DAA may contribute to maintaining MHC polymorphism, which is ancient, as supported by signatures of historical positive selection and trans-species polymorphism. Our results point to the importance of a multi-scale approach in studying MHC variation, especially in low-dispersal taxa, which are genetically structured at fine spatial scales.

Brown trout is considered a complex of incipient species, including several phylogenetic lineages, whose natural distribution in the Mediterranean area has been altered, since the beginning of the 1900s, by massive introductions of domestic strains of Atlantic origin to support fisheries. Introduced trout naturalize in new suitable environments and extensively hybridize with native populations. Here, we characterized putatively neutral and adaptive genetic variability and population structure of Mediterranean brown trout from six river catchments in central peninsular Italy, as revealed by both mitochondrial (Control Region) and nuclear (microsatellites, LDH-C1, major histocompatibility complex) markers. We quantified the admixture of wild populations with hatchery strains and evaluated the effects of domestic trout introductions on shaping population genetics. Our analyses indicated: (1) a composite picture of genetic variability in the area, with the presence of all native Mediterranean trout mitochondrial lineages (“Adriatic”, “Mediterranean”, “marmoratus”), various frequencies of allochthonous genotypes and different rates of introgression among sampling sites; (2) asymmetric mito-nuclear introgression; (3) increasing nuclear marker diversity with increasing levels of admixture across populations; (4) strong population structure coupled with relatively low effective population size. Data allowed the identification of five management units and we propose specific actions to support ongoing and future conservation strategies within the examined area.