MHC Class IIB Exon 2 Polymorphism in the Grey Partridge (Perdix perdix) Is Shaped by Selection, Recombination and Gene Conversion

Promerová, Marta; Králová, Tereza; Bryjová, Anna; Albrecht, Tomáš; Bryja, Josef

doi:10.1371/journal.pone.0069135

Cited by 24 publications

(25 citation statements)

References 89 publications

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“…The number of duplication events for MHC Class I in flamingos is larger than those reported for a large number of nonpasserine species (1–4 loci; fowl ( Gallus gallus ), Kaufman et al ., ; mallard duck ( Anas platyrhynchos ), Moon et al ., ; birds of prey, Alcaide et al ., ; turkey ( Meloeagris gallopavo ), Chaves et al ., ; red‐billed gull ( Larus scopulinus ), Cloutier et al ., ) but relatively similar to what has been found in blue petrels (8 loci; Strandh et al ., ) and red knots ( Calidris canutus ) (6 loci; Buehler et al ., ). For the MHC Class IIB, the number of loci we identified is in line with most nonpasserine species (1–3 loci; Kaufman et al ., ; Wittzell et al ., ; Alcaide et al ., , ; Strand et al ., ; Burri et al ., ; Hughes et al ., ; Kikkawa et al ., ; Juola & Dearborn, ; Strandh et al ., ; Promerová et al ., ). Overall, flamingos present a complex gene duplication history and an associated loss of gene function, with substantial differences with other avian groups.…”

Section: Discussionmentioning

confidence: 97%

Evidence of gene orthology and trans‐species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

Gillingham

Courtiol

Teixeira

et al. 2015

J of Evolutionary Biology

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The major histocompatibility complex (MHC) is a cornerstone in the study of adaptive genetic diversity. Intriguingly, highly polymorphic MHC sequences are often not more similar within species than between closely related species. Divergent selection of gene duplicates, balancing selection maintaining trans-species polymorphism (TSP) that predate speciation and parallel evolution of species sharing similar selection pressures can all lead to higher sequence similarity between species. In contrast, high rates of concerted evolution increase sequence similarity of duplicated loci within species. Assessing these evolutionary models remains difficult as relatedness and ecological similarities are often confounded. As sympatric species of flamingos are more distantly related than allopatric species, flamingos represent an ideal model to disentangle these evolutionary models. We characterized MHC Class I exon 3, Class IIB exon 2 and exon 3 of the six extant flamingo species. We found up to six MHC Class I loci and two MHC Class IIB loci. As all six species shared the same number of MHC Class IIB loci, duplication appears to predate flamingo speciation. However, the high rate of concerted evolution has prevented the divergence of duplicated loci. We found high sequence similarity between all species regardless of codon position. The latter is consistent with balancing selection maintaining TSP, as under this mechanism amino acid sites under pathogen-mediated selection should be characterized by fewer synonymous codons (due to their common ancestry) than under parallel evolution. Overall, balancing selection maintaining TSP appears to result in high MHC similarity between species regardless of species relatedness and geographical distribution.

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Section: Discussionmentioning

confidence: 97%

Evidence of gene orthology and trans‐species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

Gillingham

Courtiol

Teixeira

et al. 2015

J of Evolutionary Biology

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“…Locus‐specific screening has proceeded slowly, due in large part to high allelic similarity across diverse MHC loci and variation in MHC gene copy number. PCR‐based multilocus genotyping approaches have therefore become a popular option for conservatively estimating functional MHC diversity within and among loci in numerous bird species (Promerová et al ., , ; Canal et al ., ; Zagalska‐Neubauer et al ., ; Cloutier et al ., ; Alcaide et al ., ; Burri et al ., ), but these techniques risk incomplete isolation of functional MHC molecules. For chicken and black grouse, detailed prior knowledge of MHC genes and their flanking sequences was fundamental to the design of locus‐specific primers for the characterization of individual MHC genotypes (Worley et al ., ; Strand et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…a represent positional equivalence of these two IA loci compared to other galliform MHC class I loci; it might be a reflection of recombination/gene conversion mechanism, which can cause high sequence similarity between loci (Yeager & Hughes, ). A high incidence of recombination has been observed in MHC loci among many vertebrate taxa (Mona et al ., ; Surridge et al ., ; de Bellocq et al ., ; Orysiuk et al ., ; Promerová et al ., ), extending up to the whole MHC genomic region (Delany et al ., ; Lam et al ., ). Moreover, Chpi ‐IA1‐A and Chpi ‐IA1‐C clustered together in both trees with at least moderate support, which implies the existence of locus‐specific features for Chpi ‐IA1.…”

Section: Discussionmentioning

confidence: 98%

Molecular characterization of classical and nonclassicalMHCclassIgenes from the golden pheasant (Chrysolophus pictus)

Zeng

Zhong

et al. 2015

Int J Immunogenetics

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Classical major histocompatibility complex (MHC) class I allelic polymorphism is essential for competent antigen presentation. To improve the genotyping efforts in the golden pheasant, it is necessary to differentiate more accurately between classical and nonclassical class I molecules. In our study, all MHC class I genes were isolated from one golden pheasant based on two overlapping PCR amplifications. In total, six full-length class I nucleotide sequences (A-F) were identified, and four were novel. Two (A and C) belonged to the IA1 gene, two (B and D) were alleles derived from the IA2 gene through transgene amplification, and two (E and F) comprised a third novel locus, IA3 that was excluded from the core region of the golden pheasant MHC-B. IA1 and IA2 exhibited the broad expression profiles characteristic of classical loci, while IA3 showed no expression in multiple tissues and was therefore defined as a nonclassical gene. Phylogenetic analysis indicated that the three IA genes in the golden pheasant share a much closer evolutionary relationship than the corresponding sequences in other galliform species. This observation was consistent with high sequence similarity among them, which likely arises from the homogenizing effect of recombination. Our careful distinction between the classical and nonclassical MHC class I genes in the golden pheasant lays the foundation for developing locus-specific genotyping and establishing a good molecular marker system of classical MHC I loci.

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“…While de novo MHC sequence variation is generated by point mutation, gene conversion can generate new haplotypes by transferring sections of DNA within and across duplicated MHC loci (Spurgin et al, 2011). Gene conversion (either intra-or inter-locus) is now recognized to have a crucial role in generating and maintaining MHC diversity in many vertebrates (Reusch and Langefors, 2005;Schaschl et al, 2006), including birds (Chaves et al, 2010;Spurgin et al, 2011;Promerová et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Contrasting evolutionary histories of MHC class I and class II loci in grouse—effects of selection and gene conversion

et al. 2016

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Genes of the major histocompatibility complex (MHC) encode receptor molecules that are responsible for recognition of intracellular and extracellular pathogens (class I and class II genes, respectively) in vertebrates. Given the different roles of class I and II MHC genes, one might expect the strength of selection to differ between these two classes. Different selective pressures may also promote different rates of gene conversion at each class. Despite these predictions, surprisingly few studies have looked at differences between class I and II genes in terms of both selection and gene conversion. Here, we investigated the molecular evolution of MHC class I and II genes in five closely related species of prairie grouse (Centrocercus and Tympanuchus) that possess one class I and two class II loci. We found striking differences in the strength of balancing selection acting on MHC class I versus class II genes. More than half of the putative antigen-binding sites (ABS) of class II were under positive or episodic diversifying selection, compared with only 10% at class I. We also found that gene conversion had a stronger role in shaping the evolution of MHC class II than class I. Overall, the combination of strong positive (balancing) selection and frequent gene conversion has maintained higher diversity of MHC class II than class I in prairie grouse. This is one of the first studies clearly demonstrating that macroevolutionary mechanisms can act differently on genes involved in the immune response against intracellular and extracellular pathogens.

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MHC Class IIB Exon 2 Polymorphism in the Grey Partridge (Perdix perdix) Is Shaped by Selection, Recombination and Gene Conversion

Cited by 24 publications

References 89 publications

Evidence of gene orthology and trans‐species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

Evidence of gene orthology and trans‐species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

Molecular characterization of classical and nonclassicalMHCclassIgenes from the golden pheasant (Chrysolophus pictus)

Contrasting evolutionary histories of MHC class I and class II loci in grouse—effects of selection and gene conversion

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