Retention of functional variation despite extreme genomic erosion: MHC allelic repertoires in the Lynx genus

Abstract

BackgroundDemographic bottlenecks erode genetic diversity and may increase endangered species’ extinction risk via decreased fitness and adaptive potential. The genetic status of species is generally assessed using neutral markers, whose dynamic can differ from that of functional variation due to selection. The MHC is a multigene family described as the most important genetic component of the mammalian immune system, with broad implications in ecology and evolution. The genus Lynx includes four species differing immensely in demographic history and population size, which provides a suitable model to study the genetic consequences of demographic declines: the Iberian lynx being an extremely bottlenecked species and the three remaining ones representing common and widely distributed species. We compared variation in the most variable exon of the MHCI and MHCII-DRB loci among the four species of the Lynx genus.ResultsThe Iberian lynx was characterised by lower number of MHC alleles than its sister species (the Eurasian lynx). However, it maintained most of the functional genetic variation at MHC loci present in the remaining and genetically healthier lynx species at all nucleotide, amino acid, and supertype levels.ConclusionsSpecies-wide functional genetic diversity can be maintained even in the face of severe population bottlenecks, which caused devastating whole genome genetic erosion. This could be the consequence of divergent alleles being retained across paralogous loci, an outcome that, in the face of frequent gene conversion, may have been favoured by balancing selection.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1006-z) contains supplementary material, which is available to authorized users.

Molecular Characterization of MHC Class I Genes in Four Species of the Turdidae Family to Assess Genetic Diversity and Selection

“…Our study revealed differential expression of selection pattern in functional sequences on regions related with PBR and non-PBR of the MHC class I gene. Codons involved in peptide binding region revealed more non-synonymous substitution than synonymous (d N /d S = 1:99) in Turdus atrogularis as compared to non-peptide binding region (d N /d S = 0:884), pattern was consistent among all species tested, which might be enlightened that stronger selection pressure from intracellular pathogens than extracellular pathogens [74] It should be noted that the pooling of all alleles across loci will mostly reduce selection detection tests, so the outcomes might be conservative, but will be less prone to false positives [77,78]. Therefore, attention should be given while inferencing about the detected diversity in MHC and the possible effects of selection on individual loci.…”

Comparing raccoon major histocompatibility complex diversity in native and introduced ranges: Evidence for the importance of functional immune diversity for adaptation and survival in novel environments

“…Some degree of differentiation in supertypes present in different invasive sampling sites may be due to contrasting pathogen pressures in these sites, but may also reflect interpopulation differentiation due to demographic processes. Still, taking into account high levels Godoy, 2017;Oosterhout et al, 2006;Vlček et al, 2016) and was interpreted as the footprint of balancing selection in the form of divergent allele advantage.…”

Divergent Allele Advantage Provides a Quantitative Model for Maintaining Alleles with a Wide Range of Intrinsic Merits

“…, better protection against pathogens. A number of studies have made empirical observations consistent with DAA (She et al 1990, 1991; Dorak et al 2002; Radwan et al 2007; Mona et al 2008), with further evidence supporting this hypothesis continuing to emerge (Lenz 2011; Eizaguirre et al 2012; Froeschke and Sommer 2012; Bitarello et al 2016; Seifertová et al 2016; Marmesat et al 2017), most recently showing that heterozygotes with divergent alleles are maintained in the human population and recognize the signatures of greater numbers of peptides than genetically closer alleles (Pierini and Lenz 2018). These results support the hypothesis that divergent alleles should be preferentially maintained in the population, but what is still lacking is a quantitative model demonstrating that this mechanism will result in higher allelic diversity and a wide range of allelic fitnesses when compared to traditional AO models.…”