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Contemporary selection on MHC genes in a free-living ruminant population.

ABSTRACT: Genes within the major histocompatibility complex (MHC) are the most variable identified in vertebrates. Pathogen-mediated selection is believed to be the main force maintaining MHC diversity. However, relatively few studies have demonstrated contemporary selection on MHC genes. Here, we examine associations between MHC variation and several fitness measurements including total fitness and five fitness components, in 3400 wild Soay sheep (Ovis aries) monitored between 1989 and 2012. In terms of total fitness, measured as lifetime breeding success of all individuals born, we found haplotypes named C and D were associated with decreased and increased male total fitness respectively. In terms of fitness components, juvenile survival was associated with haplotype divergence while individual haplotypes (C, D and F) were associated with adult fitness components. Consistent with the increased male total fitness, the rarest haplotype D has increased in frequency throughout the study period more than expected under neutral expectations. Our results demonstrate that contemporary natural selection is acting on MHC class II genes in Soay sheep and that the mode of selection on specific fitness components can be different mode from selection on total fitness.

SUBMITTER: Huang W

PROVIDER: S-EPMC9306867 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Contemporary selection on MHC genes in a free-living ruminant population.

Huang Wei W Dicks Kara L KL Hadfield Jarrod D JD Johnston Susan E SE Ballingall Keith T KT Pemberton Josephine M JM

Ecology letters 20220120 4

Genes within the major histocompatibility complex (MHC) are the most variable identified in vertebrates. Pathogen-mediated selection is believed to be the main force maintaining MHC diversity. However, relatively few studies have demonstrated contemporary selection on MHC genes. Here, we examine associations between MHC variation and several fitness measurements including total fitness and five fitness components, in 3400 wild Soay sheep (Ovis aries) monitored between 1989 and 2012. In terms of ...[more]

PMID: 35050541

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Project description:BackgroundThe major histocompatibility complex (MHC) genes are vital partners in the acquired immune processes of vertebrates. MHC diversity may be directly associated with population resistance to infectious pathogens. Here, we screened for polymorphisms in exons 2 and 3 of the IA1 and IA2 genes in 12 golden pheasant populations across the Chinese mainland to characterize their genetic variation levels, to understand the effects of historical positive selection and recombination in shaping class I diversity, and to investigate the genetic structure of wild golden pheasant populations.ResultsAmong 339 individual pheasants, we identified 14 IA1 alleles in exon 2 (IA1-E2), 11 IA1-E3 alleles, 27 IA2-E2 alleles, and 28 IA2-E3 alleles. The non-synonymous substitution rate was significantly greater than the synonymous substitution rate at sequences in the IA2 gene encoding putative peptide-binding sites but not in the IA1 gene; we also found more positively selected sites in IA2 than in IA1. Frequent recombination events resulted in at least 9 recombinant IA2 alleles, in accordance with the intermingling pattern of the phylogenetic tree. Although some IA alleles are widely shared among studied populations, large variation occurs in the number of IA alleles across these populations. Allele frequency analysis across 2 IA loci showed low levels of genetic differentiation among populations on small geographic scales; however, significant genetic differentiation was observed between pheasants from the northern and southern regions of the Yangtze River. Both STRUCTURE analysis and F-statistic (F ST ) value comparison classified those populations into 2 major groups: the northern region of the Yangtze River (NYR) and the southern region of the Yangtze River (SYR).ConclusionsMore extensive polymorphisms in IA2 than IA1 indicate that IA2 has undergone much stronger positive-selection pressure during evolution. Moreover, the recombination events detected between the genes and the intermingled phylogenetic pattern indicate that interlocus recombination accounts for much of the allelic variation in IA2. Analysis of the population differentiation implied that homogenous balancing selection plays an important part in maintaining an even distribution of MHC variations. The natural barrier of the Yangtze River and heterogeneous balancing selection might help shape the NYR-SYR genetic structure in golden pheasants.

Project description:BackgroundThe effectiveness of elimination of slightly deleterious mutations depends mainly on drift and recombination frequency. Here we analyze the influence of these two factors on the strength of the purifying selection in mitochondrial and proteobacterial orthologous genes taking into account the differences in the organism lifestyles.Results(I) We found that the probability of fixation of nonsynonymous substitutions (Kn/Ks) in mitochondria is significantly lower compared to obligate intracellular bacteria and even marginally significantly lower compared to free-living bacteria. The comparison of bacteria of different lifestyles demonstrates more effective elimination of slightly deleterious mutations in (II) free-living bacteria as compared to obligate intracellular species and in (III) obligate intracellular parasites as compared to obligate intracellular symbionts. (IV) Finally, we observed that the level of the purifying selection (i.e. 1-Kn/Ks) increases with the density of mobile elements in bacterial genomes.ConclusionThis study shows that the comparison of patterns of molecular evolution of orthologous genes between ecologically different groups of organisms allow to elucidate the genetic consequences of their various lifestyles. Comparing the strength of the purifying selection among proteobacteria with different lifestyles we obtained results, which are in concordance with theoretical expectations: (II) low effective population size and level of recombination in obligate intracellular proteobacteria lead to less effective elimination of mutations compared to free-living relatives; (III) rare horizontal transmissions, i.e. effectively zero recombination level in symbiotic obligate intracellular bacteria leads to less effective purifying selection than in parasitic obligate intracellular bacteria; (IV) the increased frequency of recombination in bacterial genomes with high mobile element density leads to a more effective elimination of slightly deleterious mutations. At the same time, (I) more effective purifying selection in relatively small populations of nonrecombining mitochondria as compared to large populations of recombining proteobacteria was unexpected. We hypothesize that additional features such as the high number of protein-protein interactions or female germ-cell atresia increase evolutionary constraints and maintain the effective purifying selection in mitochondria, but more work is needed to definitely establish these additional features.

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Contemporary selection on MHC genes in a free-living ruminant population.

Publications

Contemporary selection on MHC genes in a free-living ruminant population.

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