Evolution of MHC class I genes in the European badger (Meles meles)

The major histocompatibility complex (MHC) plays a central role in the adaptive immune system and provides a good model with which to understand the evolutionary processes underlying functional genes. Trans-species polymorphism and orthology are both commonly found in MHC genes; however, mammalian MHC class I genes tend to cluster by species. Concerted evolution has the potential to homogenize different loci, whereas birth-and-death evolution can lead to the loss of orthologs; both processes result in monophyletic groups within species. Studies investigating the evolution of MHC class I genes have been biased toward a few particular taxa and model species. We present the first study of MHC class I genes in a species from the superfamily Musteloidea. The European badger (Meles meles) exhibits moderate variation in MHC class I sequences when compared to other carnivores. We identified seven putatively functional sequences and nine pseudogenes from genomic (gDNA) and complementary (cDNA) DNA, signifying at least two functional class I loci. We found evidence for separate evolutionary histories of the α1 and α2/α3 domains. In the α1 domain, several sequences from different species were more closely related to each other than to sequences from the same species, resembling orthology or trans-species polymorphism. Balancing selection and probable recombination maintain genetic diversity in the α1 domain, evidenced by the detection of positive selection and a recombination event. By comparison, two recombination breakpoints indicate that the α2/α3 domains have most likely undergone concerted evolution, where recombination has homogenized the α2/α3 domains between genes, leading to species-specific clusters of sequences. Our findings highlight the importance of analyzing MHC domains separately.     

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs

Genes of the major histocompatibility complex (MHC) play a central role in adaptive immune responses of vertebrates. They exhibit remarkable polymorphism, often crossing species boundaries with similar alleles or allelic motifs shared across species. This pattern may reflect parallel parasite‐mediated selective pressures, either favouring the long maintenance of ancestral MHC allelic lineages across successive speciation events by balancing selection (“trans‐species polymorphism”), or alternatively favouring the independent emergence of functionally similar alleles post‐speciation via convergent evolution. Here, we investigate the origins of MHC similarity across several species of dwarf and mouse lemurs (Cheirogaleidae). We examined MHC class II variation in two highly polymorphic loci (DRB, DQB) and evaluated the overlap of gut–parasite communities in four sympatric lemurs. We tested for parasite‐MHC associations across species to determine whether similar parasite pressures may select for similar MHC alleles in different species. Next, we integrated our MHC data with those previously obtained from other Cheirogaleidae to investigate the relative contribution of convergent evolution and co‐ancestry to shared MHC polymorphism by contrasting patterns of codon usage at functional vs. neutral sites. Our results indicate that parasites shared across species may select for functionally similar MHC alleles, implying that the dynamics of MHC‐parasite co‐evolution should be envisaged at the community level. We further show that balancing selection maintaining trans‐species polymorphism, rather than convergent evolution, is the primary mechanism explaining shared MHC sequence motifs between species that diverged up to 30 million years ago.     

Extensive polymorphism of the major histocompatibility complex DRA gene in Balkan donkeys: perspectives on selection and genealogy

The major histocompatibility complex (MHC) contains genes important for immune response in mammals, and these genes exhibit high polymorphism and diversity. The DRA gene, a member of the MHC class II family, is highly conserved across a large number of mammalian species, but it displays exceptionally rich sequence variations in Equidae members. We analyzed allelic polymorphism of the DRA locus in 248 donkeys sampled across the Balkan Peninsula (Albania, Bulgaria, Croatia, Macedonia, Greece and Montenegro). Five known alleles and two new alleles were identified. The new allele Eqas‐DRA*0601 was found to carry a synonymous mutation, and new allele Eqas‐DRA*0701, a non‐synonymous mutation. We further analyzed the historical selection and allele genealogy at the DRA locus in equids. Signals of positive selection obtained by various tests were ambiguous. A conservative conclusion is that DRA polymorphism occurred relatively recently and that positive selection has been acting on the DRA locus for a relatively brief period.     

The effects of historical fragmentation on major histocompatibility complex class II β and microsatellite variation in the Aegean island reptile,Podarcis erhardii

The major histocompatibility complex (MHC) plays a key role in disease resistance and is the most polymorphic gene region in vertebrates. Although habitat fragmentation is predicted to lead to a loss in MHC variation through drift, the impact of other evolutionary forces may counter this effect. Here we assess the impact of selection, drift, migration, and recombination on MHC class II and microsatellite variability in 14 island populations of the Aegean wall lizard Podarcis erhardii. Lizards were sampled from islands within the Cyclades (Greece) formed by rising sea levels as the last glacial maximum approximately 20,000 before present. Bathymetric data were used to determine the area and age of each island, allowing us to infer the corresponding magnitude and timing of genetic bottlenecks associated with island formation. Both MHC and microsatellite variation were positively associated with island area, supporting the hypothesis that drift governs neutral and adaptive variation in this system. However, MHC but not microsatellite variability declined significantly with island age. This discrepancy is likely due to the fact that microsatellites attain mutation‐drift equilibrium more rapidly than MHC. Although we detected signals of balancing selection, recombination and migration, the effects of these evolutionary processes appeared negligible relative to drift. This study demonstrates how land bridge islands can provide novel insights into the impact of historical fragmentation on genetic diversity as well as help disentangle the effects of different evolutionary forces on neutral and adaptive diversity.     

Intermediate number of major histocompatibility complex class IIB length variants relates to enlarged perivisceral fat deposits in the blunt‐head cichlid Tropheus moorii

Studying the genetic basis of host–parasite interactions represents an outstanding opportunity to observe eco‐evolutionary processes. Established candidates for such studies in vertebrates are immunogenes of the major histocompatibility complex (MHC). The MHC has been reported to reach high intra‐ and interindividual diversity, and a diverse MHC might be advantageous when facing infections from multiple parasites. However, other studies indicated that individuals with an intermediate number of MHC alleles are less infected with parasites or have other fitness advantages. In this study, we assessed the optimal number of MHC alleles in the blunt‐head cichlid Tropheus moorii from Lake Tanganyika. We investigated the influence of the interindividual variation in number of MHC length variants on parasite infection and body condition, measured by the amount of perivisceral fat reserves. Surprisingly, there was no correlation between parasite infection and number of MHC length variants or perivisceral fat deposits. However, the individual number of MHC length variants significantly correlated with the amount of perivisceral fat deposits in males, suggesting that male individuals with an intermediate number of alleles might be able to use their fat reserves more efficiently.     

Cross‐species comparison of microsatellite loci in the Culex pipiens complex and beyond

In the past, we have developed microsatellite loci from the two most common members of the Culex pipiens complex, Culex quinquefasciatus and Culex pipiens. Here we describe seven additional loci and present an extensive survey of a panel of 20 loci across most of the species and subspecies in the complex as well as in morphologically related species. Because we observed a high degree of polymorphism in the flanking regions, we designed new primers and surveyed multiple populations. We present alternate primers and discuss the cross‐species usefulness of these Culex microsatellite loci in a phylogenetic context.     

Association between the bovine major histocompatibility complex and chronic posterior spinal paresis – a form of ankylosing spondylitis – in Holstein bulls

A highly significant association was found between the bovine MHC class I antigen BoLA-A8 and a form of vertebral osteophytosis/ankylosing spondylitis known as chronic posterior spinal paresis (PSP) in Holstein bulls (P < 0.001). In a population study, restricted to unrelated bulls, BOLA-A8 was significantly associated with PSP (P= 0.0015) with a relative risk of 34.6. In a family study, one PSP bull, BoLA A8/A20, sired 13 offspring. BOLA-A8 was significantly associated with PSP (P= 0–0008). All five PSP sons inherited the A8 allele and the eight healthy sons each inherited the A20 allele. In three other families a complete association of BOLA-A8 and PSP was observed. Lod score analysis, using all available families, indicated a significant linkage between BoLA and PSP (lod score = 6–9). Based on clinical observation, pathology, age/sex predilection, and a strong association with a class I MHC molecule, this inflammatory disease appears analogous to the human condition known as ankylosing spondylitis.     

Sex‐biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor,Boa constrictor occidentalis

Abstract The knowledge of dispersal is essential to understand the ecology of any species, since population dynamics, spatial distribution and genetic structure are closely tied to patterns of movement. In this paper we estimate dispersal patterns in natural populations of the endangered snake Boa constrictor occidentalis (Serpentes, Boidae), using allozymes as genetic markers. Blood samples were obtained from a total of 120 adult individuals of nine localities from two areas, Sobremonte and Pocho, in Argentina. Only four out of a total of 24 loci were polymorphic: 6‐Pgdh‐1, Cat‐1, Ldh and Hp. The values of expected and observed mean heterozygosities, the percentage of polymorphic loci and mean number of alleles per locus for each population confirm the low levels of genetic variability in this snake. F_ST and N_em mean values were 0.0089 and 46.1 for Sobremonte and 0.0379 and 7.46 for Pocho, indicating important levels of gene flow. A comparison of F_ST between genders in both areas suggests a male‐biased dispersal, which could be explained by the characteristics of the mating system: males carry out an active mate search of receptive females, and philopatry could be selected in females due to the benefits of the familiarity with the natal area in the use of local resources.