Evolution by Recombination and Transspecies Polymorphism in the MHC Class I Gene of Xenopus laevis

Bos, David H.; Waldman, Bruce

doi:10.1093/molbev/msj016

Cited by 49 publications

(46 citation statements)

References 49 publications

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“…One possible mechanism underlying these results is the exchange of entire exons during recombination, as opposed to shorter motifs within exons. In X. laevis, at least two recombinant alleles (Xela-UAA*06 and UAA*11) have identical a1 domain sequences, but divergent a2 and a3 domains (Bos and Waldman, 2006a). Our results are consistent with this pattern, especially given that we amplified sequences from five of the six species that were identical in one domain, but differed in others.…”

Section: Discussionsupporting

confidence: 85%

“…Overall, while the number of unique MHC class I sequences within individuals in this study is striking when compared with other frogs examined to date, our results are not entirely unexpected, especially given the small percentage of frog species whose MHC genes have been characterized (Figure 1) and the diversity of ploidy levels within anurans. MHC variability is predominantly caused by the accumulation of point mutations over millions of years, with recombination, gene duplication and gene convergence generating additional allelic diversity (Parham and Ohta, 1996;Little and Parham, 1999;Bos and Waldman, 2006a). The large number of sequences recovered within individual frogs in this study may also reflect the joint effects of intraand interlocus recombination acting across several MHC class I paralogs.…”

Section: Discussionmentioning

confidence: 82%

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Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication

et al. 2012

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Comparative studies of major histocompatibility complex (MHC) genes across vertebrate species can reveal the evolutionary processes that shape the structure and function of immune regulatory proteins. In this study, we characterized MHC class I sequences from six frog species representing three anuran families (Hylidae, Centrolenidae and Ranidae). Using cDNA from our focal species, we amplified a total of 79 unique sequences spanning exons 2-4 that encode the extracellular domains of the functional alpha chain protein. We compared intra-and interspecific nucleotide and amino-acid divergence, tested for recombination, and identified codon sites under selection by estimating the rate of non-synonymous to synonymous substitutions with multiple codon-based maximum likelihood methods. We determined that positive (diversifying) selection was acting on specific amino-acid sites located within the domains that bind pathogen-derived peptides. We also found significant signals of recombination across the physical distance of the genes. Finally, we determined that all the six species expressed two or three putative classical class I loci, in contrast to the single locus condition of Xenopus laevis. Our results suggest that MHC evolution in anurans is a dynamic process and that variation in numbers of loci and genetic diversity can exist among taxa. Thus, the accumulation of genetic data for more species will be useful in further characterizing the relative importance of processes such as selection, recombination and gene duplication in shaping MHC loci among amphibian lineages.

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Section: Discussionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 82%

Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication

et al. 2012

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“…Sharing of MHC alleles between species from the same genus has been found in several recently diverged taxonomic groups, such as Xenopus frogs (Bos and Waldman, 2006), Spheniscus penguins (Bollmer et al, 2007;Kikkawa et al, 2009), equids (Kamath and Getz, 2011) and primates (Doxiadis et al, 2006). The divergence between all three Tympanuchus species likely occurred within the last 0.5-2 million years, and in areas of geographic overlap, hybridisation has been observed between T. cupido and two other Tympanuchus grouse (Galla and Johnson, 2015).…”

Section: Discussionmentioning

confidence: 95%

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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“…However, relatively few studies have focused on the evolution of amphibian MHC class I genes, and those few studies have involved a limited number of amphibian species, mainly Ambystoma mexicanum in the Caudata [36] and two closely related Pipidae species ( Xenopus lavies and X. (Silurana) tropicalis ) in the Anura [37-39]. These studies revealed that (1) Urodela ( Ambystoma ) have multiple MHC class I loci [36], whereas the Anura (Pipidae and Ranidae) have only one [37-41]; it is possible that the number of MHC class I loci increased after the Urodela and Anura but before the Pipidae and Ranidae diverged [40].…”

Section: Introductionmentioning

confidence: 99%

Evolution by selection, recombination, and gene duplication in MHC class I genes of two Rhacophoridae species

et al. 2013

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BackgroundComparison of major histocompatibility complex (MHC) genes across vertebrate species can reveal molecular mechanisms underlying the evolution of adaptive immunity-related proteins. As the first terrestrial tetrapods, amphibians deserve special attention because of their exposure to probably increased spectrum of microorganisms compared with ancestral aquatic fishes. Knowledge regarding the evolutionary patterns and mechanisms associated with amphibian MHC genes remains limited. The goal of the present study was to isolate MHC class I genes from two Rhacophoridae species (Rhacophorus omeimontis and Polypedates megacephalus) and examine their evolution.ResultsWe identified 27 MHC class I alleles spanning the region from exon 2 to 4 in 38 tree frogs. The available evidence suggests that these 27 sequences all belong to classical MHC class I (MHC Ia) genes. Although several anuran species only display one MHC class Ia locus, at least two or three loci were observed in P. megacephalus and R. omeimontis, indicating that the number of MHC class Ia loci varies among anuran species. Recombination events, which mainly involve the entire exons, played an important role in shaping the genetic diversity of the 27 MHC class Ia alleles. In addition, signals of positive selection were found in Rhacophoridae MHC class Ia genes. Amino acid sites strongly suggested by program to be under positive selection basically accorded with the putative antigen binding sites deduced from crystal structure of human HLA. Phylogenetic relationships among MHC class I alleles revealed the presence of trans-species polymorphisms.ConclusionsIn the two Rhacophoridae species (1) there are two or three MHC class Ia loci; (2) recombination mainly occurs between the entire exons of MHC class Ia genes; (3) balancing selection, gene duplication and recombination all contribute to the diversity of MHC class Ia genes. These findings broaden our knowledge on the evolution of amphibian MHC systems.

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Evolution by Recombination and Transspecies Polymorphism in the MHC Class I Gene of Xenopus laevis

Cited by 49 publications

References 49 publications

Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication

Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication

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

Evolution by selection, recombination, and gene duplication in MHC class I genes of two Rhacophoridae species

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