Evidence for selection maintaining MHC diversity in a rodent species despite strong density fluctuations

Abstract

Strong spatiotemporal variation in population size often leads to reduced genetic diversity limiting the adaptive potential of individual populations. Key genes of adaptive variation are encoded by the immune genes of the major histocompatibility complex (MHC) playing an essential role in parasite resistance. How MHC variation persists in rodent populations that regularly experience population bottlenecks remains an important topic in evolutionary genetics. We analysed the consequences of strong population fluctuations on MHC class II DRB exon 2 diversity in two distant common vole (Microtus arvalis) populations in three consecutive years using a high-throughput sequencing approach. In 143 individuals, we detected 25 nucleotide alleles translating into 14 unique amino acid MHC alleles belonging to at least three loci. Thus, the overall allelic diversity and amino acid distance among the remaining MHC alleles, used as a surrogate for the range of pathogenic antigens that can be presented to T-cells, are still remarkably high. Both study populations did not show significant population differentiation between years, but significant differences were found between sites. We concluded that selection processes seem to be strong enough to maintain moderate levels of MHC diversity in our study populations outcompeting genetic drift, as the same MHC alleles were conserved between years. Differences in allele frequencies between populations might be the outcome of different local parasite pressures and/or genetic drift. Further understanding of how pathogens vary across space and time will be crucial to further elucidate the mechanisms maintaining MHC diversity in cyclic populations.

Host-parasite interactions in non-native invasive species are dependent on the levels of standing genetic variation at the immune locus

“…Genes that compose the major histocompatibility complex (MHC) capture an essential fraction of adaptive genetic variation underpinning resistance to pathogens [15,16] and have proved to be useful in examining the adaptive potential of populations in mammalian species [17][18][19][20]. The high polymorphism of MHC has been demonstrated to be maintained by balancing selection driven by pathogens [21][22][23][24].…”

A quantitative and qualitative comparison of illumina MiSeq and 454 amplicon sequencing for genotyping the highly polymorphic major histocompatibility complex (MHC) in a non-model species

“…Although it has been suggested that MiSeq improves our ability to discern true alleles from artefacts in species with many MHC genes [ 25 ], this has yet to be tested directly. This is an important omission as there is still a great deal of research being published that has used 454 for MHC genotyping [ 31 , 35 – 39 ]. Thus, it is valuable to determine, in species with many MHC gene copies, how 454 and MiSeq genotyping compares.…”

The role of demographic history and selection in shaping genetic diversity of the Galápagos penguin (Spheniscus mendiculus)

“…The active role of selection during bottleneck events has been previously demonstrated in experimental populations of Drosophila melanogaster [45,46]. A few other studies have found recent signatures of selection at MHC loci in natural populations despite the presence of bottleneck events (e.g., [36,37,38,39,40,41]). Our study adds, therefore, to the body of literature suggesting that selection can potentially mitigate the effects of genetic drift during demographic bottlenecks.…”

“…Since demographic bottlenecks result in a significant decrease in N e , genetic drift would tend to outweigh the effect of balancing selection on MHC variation [34,35]. While most studies suggest that MHC loci become effectively neutral during population bottlenecks (e.g., [12,25,26,28]), some studies have found that balancing selection can outweigh genetic drift and produce recent signatures of selection [36,37,38,39,40,41]. Thus, there is still considerable debate about the relative roles that natural selection and genetic drift may play in shaping genetic diversity during population bottlenecks [2,42,43,44,45,46].…”