Mhc class II diversity and balancing selection in greater prairie-chickens

Abstract Background Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classical MHC genes show high polymorphism and are under strong balancing selection, as their products trigger the adaptive immune response in vertebrates. Here, we assess the allelic diversity and patterns of selection for MHC class I and class II loci in a threatened shorebird with highly flexible mating and parental care behaviour, the Snowy Plover (Charadrius nivosus) across its broad geographic range. Results We determined the allelic and nucleotide diversity for MHC class I and class II genes using samples of 250 individuals from eight breeding population of Snowy Plovers. We found 40 alleles at MHC class I and six alleles at MHC class II, with individuals carrying two to seven different alleles (mean 3.70) at MHC class I and up to two alleles (mean 1.45) at MHC class II. Diversity was higher in the peptide-binding region, which suggests balancing selection. The MHC class I locus showed stronger signatures of both positive and negative selection than the MHC class II locus. Most alleles were present in more than one population. If present, private alleles generally occurred at very low frequencies in each population, except for the private alleles of MHC class I in one island population (Puerto Rico, lineage tenuirostris). Conclusion Snowy Plovers exhibited an intermediate level of diversity at the MHC, similar to that reported in other Charadriiformes. The differences found in the patterns of selection between the class I and II loci are consistent with the hypothesis that different mechanisms shape the sequence evolution of MHC class I and class II genes. The rarity of private alleles across populations is consistent with high natal and breeding dispersal and the low genetic structure previously observed at neutral genetic markers in this species.

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Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae)

Immunogenetics ◽

10.1007/s00251-006-0085-6 ◽

2006 ◽

Vol 58 (2-3) ◽

pp. 191-202 ◽

Cited By ~ 51

Author(s):

J. Bryja ◽

M. Galan ◽

N. Charbonnel ◽

J. F. Cosson

Keyword(s):

Mhc Class Ii ◽

Balancing Selection ◽

Class Ii ◽

Species Evolution

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Gene duplication and evidence for balancing selection acting on MHC class II DAA gene of the half-smooth tongue sole (Cynoglossus semilaevis)

Marine Genomics ◽

10.1016/j.margen.2010.08.004 ◽

2010 ◽

Vol 3 (2) ◽

pp. 117-123 ◽

Cited By ~ 4

Author(s):

Tian-jun Xu ◽

Yue-na Sun ◽

Ri-xin Wang

Keyword(s):

Gene Duplication ◽

Mhc Class Ii ◽

Balancing Selection ◽

Class Ii ◽

Cynoglossus Semilaevis ◽

Tongue Sole ◽

Half Smooth Tongue Sole

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Genetic variation and balancing selection at MHC class II exon 2 in cultured stocks and wild populations of orange-spotted grouper (Epinephelus coioides)

Genetics and Molecular Research ◽

10.4238/2012.november.12.4 ◽

2012 ◽

Vol 11 (4) ◽

pp. 3869-3881 ◽

Cited By ~ 2

Author(s):

Z.N. Meng ◽

S. Yang ◽

B. Fan ◽

L. Wang ◽

H.R. Lin

Keyword(s):

Genetic Variation ◽

Mhc Class Ii ◽

Balancing Selection ◽

Class Ii ◽

Epinephelus Coioides ◽

Wild Populations ◽

Exon 2

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MHC reflects fine-scale habitat structure in white-tailed eagles Haliaeetus albicilla

Journal of Heredity ◽

10.1093/jhered/esab026 ◽

2021 ◽

Author(s):

Piotr Minias ◽

Aleksandra Janiszewska ◽

Ewa Pikus ◽

Tomasz Zadworny ◽

Dariusz Anderwald

Keyword(s):

Mhc Class I ◽

Mhc Class Ii ◽

Habitat Structure ◽

Balancing Selection ◽

Strong Support ◽

Class Ii ◽

Class I ◽

Fluctuating Selection ◽

Haliaeetus Albicilla ◽

Habitat Variation

Abstract The Major Histocompatibility Complex (MHC) genes code for key immune receptors responsible for recognition of intra- and extra-cellular pathogens (MHC class I and class II, respectively). It was hypothesized that MHC polymorphism can be maintained via fluctuating selection resulting from between-habitat variation in pathogen regimes. We examined associations between MHC class I and class II genes and habitat structure in an apex avian predator, the white-tailed eagle Haliaeetus albicilla. We genotyped MHC class I and class II genes in ca. 150 white-tailed eagle chicks from nearly one hundred nesting territories distributed across three distinct populations in Poland. Habitat structure was quantified at the levels of foraging territories and directly at the nest sites. We found strong support for associations of habitat traits with diversity and allelic composition at the MHC class II. Forest area within territory and forest productivity were identified as the major habitat predictors of MHC class II polymorphism, while other habitat traits (distance to nearest open water, grassland and water area within territory or understory presence) showed fewer associations with class II alleles. In contrast, there was little support for associations between MHC class I genes and habitat structure. All significant associations were apparent at the within- rather than between-population level. Our results suggest that extra-cellular (rather than intra-cellular) pathogens may exert much stronger selective pressure on the white-tailed eagle. Associations of habitat structure with MHC class II may reflect fluctuating (balancing) selection which maintains MHC diversity within populations.

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Correction to: Balancing selection versus allele and supertype turnover in MHC class II genes in guppies

Heredity ◽

10.1038/s41437-021-00407-y ◽

2021 ◽

Author(s):

Magdalena Herdegen-Radwan ◽

Karl P. Phillips ◽

Wieslaw Babik ◽

Ryan S. Mohammed ◽

Jacek Radwan

Keyword(s):

Mhc Class Ii ◽

Balancing Selection ◽

Class Ii ◽

Mhc Class Ii Genes

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Ancestral Polymorphism of Mhc Class II Genes in Mice: Implications for Balancing Selection and the Mammalian Molecular Clock

Genetics ◽

10.1093/genetics/146.2.655 ◽

1997 ◽

Vol 146 (2) ◽

pp. 655-668 ◽

Cited By ~ 1

Author(s):

Scott V Edwards ◽

Kye Chesnut ◽

Yoko Satta ◽

Edward K Wakeland

Keyword(s):

Mhc Class Ii ◽

Evolutionary Dynamics ◽

Balancing Selection ◽

Relative Rate ◽

Synonymous Substitution ◽

Class Ii ◽

Coalescent Simulation ◽

Ancestral Polymorphism ◽

Mammalian Genes ◽

Similar Sample

To investigate the evolutionary dynamics at Mhc class II DR genes of mice (genus Mus), we sequenced the peptide binding regions (PBRs) of 41 DRB (=Eβ) genes and eight DRA (=Eα) genes from 15 strains representing eight species. As expected trees of these PBR sequences imply extensive maintenance of ancestral DRB alleles across species. We use a coalescent simulation model to show that the number of interspecific coalescent events (c) observed on these trees was higher than the number expected for neutral genealogies and similar sample sizes and is more consistent with balancing selection than with neutrality. Patterns of ancestral polymorphism in mouse DRB alleles were also used to examine the tempo of synonymous substitution in the PBR of mouse class II genes. Both absolute and relative rate tests on DRA and DRB genes imply increased substitution rates at two- and fourfold degnerate sites of mice and rats relative to primates, and decreased rates for the DRB genes of primates relative to ungulate and carnivore relatives. Thus rates of synonymous substitution at Mhc DR genes in mammals appear to be subject to generation time effects in ways similar to those found at other mammalian genes.

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