Abstract
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.
Highlights
Because 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
The estimated level of misassignment was about two times higher than reported previously [40,47], it was still low enough to ensure that misassigned reads are rare, and as such will not affect the outcome of genotyping, which requires an allele to be present in multiple reads
We demonstrated an extreme complexity of the MHC class IIB in the collared flycatchers, our estimates point to the presence of at least nine expressed and fifteen pseudogene loci, but this latter number is highly uncertain and likely to be a gross underestimate of the actual number of pseudogene loci
Summary
Because 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. The products of the MHC genes are involved in triggering the adaptive immune response against pathogens [1], and may play a role in mate choice and individual recognition (reviewed in [3,4]) Because of their functional significance, MHC class I and II genes have been the subject of continuous interest in the fields of ecology, evolution and conservation (reviewed in [2,3,5,6]). In some taxa, concerted evolution through gene conversion appears to be important, and recombination may generate additional variation [13,14,15,16] These processes may be manifested at the population level by the coexistence of haplotypes that differ in the number of loci [17,18]. A comprehensive understanding of the actual mechanisms that generate and maintain copy number variation in the MHC requires substantial population genomic information from multiple species
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