Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene

Hughes, Colin; Miles, Shana; Walbroehl, Jaclyn M.

doi:10.1007/s00251-008-0287-1

Cited by 45 publications

(32 citation statements)

References 73 publications

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“…In quail [34], red-winged blackbird [42,48] and the zebra finch, there are multiple Class II genes. Most non-passerine species, in contrast, appear to have only between one and three loci [60,62,63]. Given the derived phylogenetic position of passerines [64], these patterns imply that in terms of Class II genes, a minimal MHC may be ancestral for birds [60,62].…”

Section: Discussionmentioning

confidence: 99%

Gene duplication and fragmentation in the zebra finch major histocompatibility complex

et al. 2010

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BackgroundDue to its high polymorphism and importance for disease resistance, the major histocompatibility complex (MHC) has been an important focus of many vertebrate genome projects. Avian MHC organization is of particular interest because the chicken Gallus gallus, the avian species with the best characterized MHC, possesses a highly streamlined minimal essential MHC, which is linked to resistance against specific pathogens. It remains unclear the extent to which this organization describes the situation in other birds and whether it represents a derived or ancestral condition. The sequencing of the zebra finch Taeniopygia guttata genome, in combination with targeted bacterial artificial chromosome (BAC) sequencing, has allowed us to characterize an MHC from a highly divergent and diverse avian lineage, the passerines.ResultsThe zebra finch MHC exhibits a complex structure and history involving gene duplication and fragmentation. The zebra finch MHC includes multiple Class I and Class II genes, some of which appear to be pseudogenes, and spans a much more extensive genomic region than the chicken MHC, as evidenced by the presence of MHC genes on each of seven BACs spanning 739 kb. Cytogenetic (FISH) evidence and the genome assembly itself place core MHC genes on as many as four chromosomes with TAP and Class I genes mapping to different chromosomes. MHC Class II regions are further characterized by high endogenous retroviral content. Lastly, we find strong evidence of selection acting on sites within passerine MHC Class I and Class II genes.ConclusionThe zebra finch MHC differs markedly from that of the chicken, the only other bird species with a complete genome sequence. The apparent lack of synteny between TAP and the expressed MHC Class I locus is in fact reminiscent of a pattern seen in some mammalian lineages and may represent convergent evolution. Our analyses of the zebra finch MHC suggest a complex history involving chromosomal fission, gene duplication and translocation in the history of the MHC in birds, and highlight striking differences in MHC structure and organization among avian lineages.

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Section: Discussionmentioning

confidence: 99%

Gene duplication and fragmentation in the zebra finch major histocompatibility complex

et al. 2010

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“…Some species, such as chicken or parrots, have an extremely small, compact MHC, dubbed "the minimal essential MHC" [28,29]. Other birds, such as owls [30], exhibit more complex MHC structure with multiple loci that may retain orthologous relationships over long periods of evolutionary time, a situation resembling the patterns observed in mammals [7,12].…”

Section: Introductionmentioning

confidence: 99%

454 sequencing reveals extreme complexity of the class II Major Histocompatibility Complex in the collared flycatcher

et al. 2010

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BackgroundBecause of their functional significance, the Major Histocompatibility Complex (MHC) class I and II genes have been the subject of continuous interest in the fields of ecology, evolution and conservation. In some vertebrate groups MHC consists of multiple loci with similar alleles; therefore, the multiple loci must be genotyped simultaneously. In such complex systems, understanding of the evolutionary patterns and their causes has been limited due to challenges posed by genotyping.ResultsHere we used 454 amplicon sequencing to characterize MHC class IIB exon 2 variation in the collared flycatcher, an important organism in evolutionary and immuno-ecological studies. On the basis of over 152,000 sequencing reads we identified 194 putative alleles in 237 individuals. We found an extreme complexity of the MHC class IIB in the collared flycatchers, with our estimates pointing to the presence of at least nine expressed loci and a large, though difficult to estimate precisely, number of pseudogene loci. Many similar alleles occurred in the pseudogenes indicating either a series of recent duplications or extensive concerted evolution. The expressed alleles showed unambiguous signals of historical selection and the occurrence of apparent interlocus exchange of alleles. Placing the collared flycatcher's MHC sequences in the context of passerine diversity revealed transspecific MHC class II evolution within the Muscicapidae family.Conclusions454 amplicon sequencing is an effective tool for advancing our understanding of the MHC class II structure and evolutionary patterns in Passeriformes. We found a highly dynamic pattern of evolution of MHC class IIB genes with strong signals of selection and pronounced sequence divergence in expressed genes, in contrast to the apparent sequence homogenization in pseudogenes. We show that next generation sequencing offers a universal, affordable method for the characterization and, in perspective, genotyping of MHC systems of virtually any complexity.

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“…by having only one or two class IIb genes (e.g., parrotlets, Forpus passerinus,Hughes et al 2008; several penguin species,Tsuda et al 2001), including some…”

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

et al. 2009

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The major histocompatibility complex (Mhc) of domestic chickens has been characterized as small and relatively simple compared with that of mammals. However, there is growing evidence that the Mhc of many bird lineages may be more complex, even within the Order Galliformes. In this study, we measured genetic variation and balancing selection at Mhc loci in another galliform, the greater prairie-chicken. We cloned and sequenced a 239 bp fragment of Mhc Class II beta-chain (BLB) exon 2 in 14 individuals. There was a total of 10 unique sequences and a minimum of four BLB loci. The d(N)/d(S) ratio at peptide-binding codons was significantly greater than one, suggesting balancing selection is acting on the BLB. We also recovered two YLB sequences, which clustered tightly with YLB sequences from three other species: domestic chicken, black grouse and common quail. The relatively large number of loci revealed in our study suggests that even closely related galliforms differ in the level of Mhc variation and structure.

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Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene

Cited by 45 publications

References 73 publications

Gene duplication and fragmentation in the zebra finch major histocompatibility complex

Gene duplication and fragmentation in the zebra finch major histocompatibility complex

454 sequencing reveals extreme complexity of the class II Major Histocompatibility Complex in the collared flycatcher

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

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