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Theory of local adaptation predicts that nonadapted migrants will suffer increased costs compared to local residents. Ultimately this process can result in the reduction of gene flow and culminate in speciation. Here, we experimentally investigated the relative fitness of migrants in foreign habitats, focusing on diverging lake and river ecotypes of three-spined sticklebacks. A reciprocal transplant experiment performed in the field revealed asymmetric costs of migration: whereas mortality of river fish was increased under lake conditions, lake migrants suffered from reduced growth relative to river residents. Selection against migrants thus involved different traits in each habitat but generally contributed to bidirectional reduction in gene flow. Focusing particularly on the parasitic environments, migrant fish differed from resident fish in the parasite community they harboured. This pattern correlated with both cellular phenotypes of innate immunity as well as with allelic variation at the genes of the major histocompatibility complex. In addition to showing the costs of migration in three-spined sticklebacks, this study highlights the role of asymmetric selection particularly from parasitism in genotype sorting and in the emergence of local adaptation.

Highlights: • We investigated in vitro responses of stickleback leukocytes to parasite antigens. • In vitro responses decreased from generalist to specialist parasites. • Responses decreased from Gasterosteusaculeatus not infecting to infecting parasites. • Leukocyte response was increased with parasite prevalence in the natural habitat. • Immunogenicity of antigens was increased with parasite prevalence as well. Helminth parasites of teleost fish have evolved strategies to evade and manipulate the immune responses of their hosts. Responsiveness of fish host immunity to helminth antigens may therefore vary depending on the degree of host-parasite counter-adaptation. Generalist parasites, infective for a number of host species, might be unable to adapt optimally to the immune system of a certain host species, while specialist parasites might display high levels of adaptation to a particular host species. The degree of adaptations may further differ between sympatric and allopatric host-parasite combinations. Here, we test these hypotheses by in vitro exposure of head kidney leukocytes from three-spined sticklebacks (Gasterosteus aculeatus) to antigens from parasites with a broad fish host range (Diplostomum pseudospathaceum, Triaenophorus nodulosus), a specific fish parasite of cyprinids (Ligula intestinalis) and parasites highly specific only to a single fish species as second intermediate host (Schistocephalus pungitii, which does not infect G. aculeatus, and Schistocephalus solidus, infecting G. aculeatus). In vitro responses of stickleback leukocytes to S. solidus antigens from six European populations, with S. solidus prevalence from <1% to 66% were tested in a fully crossed experimental design. Leukocyte cultures were analysed by means of flow cytometry and a chemiluminescence assay to quantify respiratory burst activity. We detected decreasing magnitudes of in vitro responses to antigens from generalist to specialist parasites and among specialists, from paras

The major histocompatibility complex (MHC)-mediated adaptive immune system is the hallmark of gnathostome immune defence. Recent work suggests that cod-like fishes (Gadidae) lack important components of the MHC class II mediated immunity. Here, we report a putative independent loss of functionality of this pathway in another species, the pipefish Syngnathus typhle, that belongs to a distantly related fish family (Syngnathidae). In a deep transcriptome sequencing approach comprising several independent normalized and non-normalized expressed sequence tag (EST) libraries with approximately 7.5 × 108 reads, sequenced with two next generation platforms (454 and Illumina), we were unable to identify MHC class IIα/β genes as well as genes encoding associated receptors. Along with the recent findings in cod, our results suggest that immune systems of the Euteleosts may be more variable than previously assumed.

The immunologically important major histocompatibility complex (MHC) harbors some of the most polymorphic genes in vertebrates. These genes presumably evolve under parasite-mediated selection and frequently show inconsistent allelic genealogies, where some alleles are more similar between species than within species. This phenomenon is thought to arise either from convergent evolution under parallel selection or from the preservation of ancient allelic lineages beyond speciation events (trans-species polymorphism, TSP). Here, we examine natural populations of two sympatric stickleback species (Gasterosteus aculeatus and Pungitius pungitius) to investigate the contribution of these two mechanisms to the evolution of inconsistent allelic genealogies at the MHC. Overlapping parasite taxa between the two host species in three different habitats suggest contemporary parallel selection on the MHC genes. Accordingly, we detected a lack of species-specific phylogenetic clustering in the immunologically relevant antigen-binding residues of the MHC IIB genes which contrasted with the rest of the coding and noncoding sequence. However, clustering was not habitat-specific and a codon-usage analysis revealed patterns of similarity by descent. In this light, common descent via TSP, in combination with intraspecies gene conversion, rather than convergent evolution is the more strongly supported scenario for the inconsistent genealogy at the MHC.

The genes of the major histocompatibility complex are the most polymorphic genes in vertebrates, with more than 1,000 alleles described in human populations. How this polymorphism is maintained, however, remains an evolutionary puzzle. Major histocompatibility complex genes have a crucial function in the adaptive immune system by presenting parasite-derived antigens to T lymphocytes. Because of this function, varying parasite-mediated selection has been proposed as a major evolutionary force for maintaining major histocompatibility complex polymorphism. A necessary prerequisite of such a balancing selection process is rapid major histocompatibility complex allele frequency shifts resulting from emerging selection by a specific parasite. Here we show in six experimental populations of sticklebacks, each exposed to one of two different parasites, that only those major histocompatibility complex alleles providing resistance to the respective specific parasite increased in frequency in the next host generation. This result demonstrates experimentally that varying parasite selection causes rapid adaptive evolutionary changes, thus facilitating the maintenance of major histocompatibility complex polymorphism.

Polymorphicgenesofthemajorhistocompatibilitycomplex(MHC)areregardedasessential genes for individual fitness under conditions of natural and sexual selection. To test this hypothesis, we investigated the ultimate individual fitness trait — that of reproductive success. We used three-spined sticklebacks (Gasterosteus aculeatus) in seminatural enclosures, located in natural breeding areas where the experimental fish had been caught. During their reproductive period, fish were exposed continuously to their natural sympatric parasites. By genotyping almost 4000 eggs with nine microsatellites, we determined parenthood and inferred female mating decision. We found that with reference to their own MHC profile, female sticklebacks preferred to mate with males sharing an intermediate MHC diversity. In addition, males with a specific MHC haplotype were bigger and better at fighting a common parasite (Gyrodactylus sp.). This translated directly into Darwinian fitness since fish harbouring this specific MHC haplotype were more likely to be chosen and had a higher reproductive output. We conclude that females also based their mating decision on a specific MHChaplotype conferring resistance against a common parasite. This identifies and supports ‘good genes’. We argue that such an interaction between host and parasite driving assortative mating is not only a prerequisite for negative frequency-dependent selection — a potential mechanism to explain the maintenance of MHC polymorphism, but also potentially speciation.

To investigate and disentangle the role of major histocompatibility complex (MHC)‐based ‘good genes' and ‘compatible genes' in mate choice, three‐spined sticklebacks Gasterosteus aculeatus with specific MHC IIB genotypes were allowed to reproduce in an outdoor enclosure system. Here, fish were protected from predators but encountered their natural parasites. Mate choice for an intermediate genetic distance between parental MHC genotypes was observed, which would result in intermediate diversity in the offspring, but no mate choice based on good genes was found under the current semi‐natural conditions. Investigation of immunological variables revealed that the less‐specific innate immune system was more active in individuals with a genetically more divergent MHC allele repertoire. This suggests the need to compensate for an MHC‐diminished T‐cell repertoire and potentially explains the observed mate choice for intermediate MHC genetic distance. The present findings support a general pattern of mate choice for intermediate MHC diversity (i.e. compatible genes). In addition, the potentially dynamic role of MHC good genes in mate choice under different parasite pressures is discussed in the light of present and previous results.

In vertebrates, genes of the major histocompatibility complex (MHC), with their pronounced polymorphism, potentially represent outstanding examples for the selective advantages of genetic diversity (1). Theoretical models predicted that, within an individual, MHC alleles can be subjected to two opposing selective forces, resulting in an optimal number of genes at intermediate individual MHC diversity (2, 3). Diversifying selection increases heterozygosity and enables wider recognition of pathogens (4). This process is opposed by the need to delete T cells that react with self peptide–MHC combinations (5) from the repertoire, which has been proposed as a possible mechanism constraining expansion of MHC genes. Because too high MHC diversity might delimit T cell diversity, it might also impose limitations on the efficiency of pathogen recognition. However, empirical evidence demonstrating fitness benefits in terms of parasite resistance caused by this type of optimal MHC diversity has been lacking. Therefore, we tested whether three-spined sticklebacks (Gasterosteus aculeatus L.) carrying an intermediate level of individual MHC diversity also displayed the strongest level of resistance against parasite infection. Sticklebacks are particularly suited to test MHC optimality, because MHC class II genotypes can differ markedly in the number of MHC class IIB alleles (6). We caught fish from an outbred population and used these to breed six sibships of immunologically naïve fish (i.e., they had no previous contact to parasites). Immunogenetic diversity ranged from three to nine MHC class IIB alleles found in reverse-transcribed messenger RNA (mRNA) [see (6) for details on genotyping]. The MHC genotypes within these sibships segregated above and below the hypothesized optimal number of ∼5 MHC class IIB alleles, which had previously been estimated in an epidemiological field survey (7). In individual infection treatments, fish from all sibships were simultaneously exposed to t