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Red Queen Processes Drive Positive Selection on Major Histocompatibility Complex (MHC) Genes.

ABSTRACT: Major Histocompatibility Complex (MHC) genes code for proteins involved in the incitation of the adaptive immune response in vertebrates, which is achieved through binding oligopeptides (antigens) of pathogenic origin. Across vertebrate species, substitutions of amino acids at sites responsible for the specificity of antigen binding (ABS) are positively selected. This is attributed to pathogen-driven balancing selection, which is also thought to maintain the high polymorphism of MHC genes, and to cause the sharing of allelic lineages between species. However, the nature of this selection remains controversial. We used individual-based computer simulations to investigate the roles of two phenomena capable of maintaining MHC polymorphism: heterozygote advantage and host-pathogen arms race (Red Queen process). Our simulations revealed that levels of MHC polymorphism were high and driven mostly by the Red Queen process at a high pathogen mutation rate, but were low and driven mostly by heterozygote advantage when the pathogen mutation rate was low. We found that novel mutations at ABSs are strongly favored by the Red Queen process, but not by heterozygote advantage, regardless of the pathogen mutation rate. However, while the strong advantage of novel alleles increased the allele turnover rate, under a high pathogen mutation rate, allelic lineages persisted for a comparable length of time under Red Queen and under heterozygote advantage. Thus, when pathogens evolve quickly, the Red Queen is capable of explaining both positive selection and long coalescence times, but the tension between the novel allele advantage and persistence of alleles deserves further investigation.

SUBMITTER: Ejsmond MJ

PROVIDER: S-EPMC4658181 | biostudies-literature | 2015 Nov

REPOSITORIES: biostudies-literature

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Red Queen Processes Drive Positive Selection on Major Histocompatibility Complex (MHC) Genes.

Ejsmond Maciej Jan MJ Radwan Jacek J

PLoS computational biology 20151124 11

Major Histocompatibility Complex (MHC) genes code for proteins involved in the incitation of the adaptive immune response in vertebrates, which is achieved through binding oligopeptides (antigens) of pathogenic origin. Across vertebrate species, substitutions of amino acids at sites responsible for the specificity of antigen binding (ABS) are positively selected. This is attributed to pathogen-driven balancing selection, which is also thought to maintain the high polymorphism of MHC genes, and t ...[more]

PMID: 26599213

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Project description:Urban sprawl is one of the most common landscape alterations occurring worldwide, and there is a growing list of species that are recognised to have adapted to urban life. To be successful, processes of urban colonization by wildlife require a broad spectrum of phenotypic (e.g., behavioural or physiological) adjustments, but evidence for genetic adaptations is much scarcer. One hypothesis proposes that different pathogen-driven selective pressures between urban and non-urban landscapes leads to adaptations in host immune genes. Here, we examined urbanization-related differentiation at the key pathogen-recognition genes of vertebrate adaptive immunity-the major histocompatibility complex (MHC)-in a common waterbird, the Eurasian coot (Fulica atra). Samples were collected from an old urban population (established before the 1950s), a new urban population (established in the 2000s), and two rural populations from central Poland. We found strong significant divergence (as measured with Jost's D) at the MHC class II between the old urban population and the remaining (new urban and rural) populations. Also, there was a moderate, but significant divergence at the MHC between the new urban population and two rural populations, while no divergence was found between the two rural populations. The total number of MHC alleles and the number of private (population-specific) MHC alleles was lower in old urban populations, as compared to the rural ones. These patterns of differentiation at the MHC were not consistent with patterns found for neutral genetic markers (microsatellites), which showed few differences between the populations. Our results indicate that MHC allele composition depended on the level of anthropogenic disturbance and the time which passed since urban colonization, possibly due to the processes of genotype sorting and local adaptation. As such, our study contributes to the understanding of genetic mechanisms associated with urbanization processes in wildlife.

Dataset Information

Red Queen Processes Drive Positive Selection on Major Histocompatibility Complex (MHC) Genes.

Publications

Red Queen Processes Drive Positive Selection on Major Histocompatibility Complex (MHC) Genes.

Similar Datasets

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