Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations

Abstract

The major histcompatibility complex (MHC) is a vital component of the adaptive immune system in all vertebrates. This study is the first to characterize MHC class I (MHC-I) in blue tits (Cyanistes caeruleus), and we use MHC-I exon 3 sequence data from individuals originating from three locations across Europe: Spain, the Netherlands to Sweden. Our phylogeny of the 17 blue tit MHC-I alleles contains one allele cluster with low nucleotide diversity compared to the remaining more diverse alleles. We found a significant evidence for balancing selection in the peptide-binding region in the diverse allele group only. No separation according to geographic location was found in the phylogeny of alleles. Although the number of MHC-I loci of the blue tit is comparable to that of other passerine species, the nucleotide diversity of MHC-I appears to be much lower than that of other passerine species, including the closely related great tit (Parus major) and the severely inbred Seychelles warbler (Acrocephalus sechellensis). We believe that this initial MHC-I characterization in blue tits provides an important step towards understanding the mechanisms shaping MHC-I diversity in natural populations.

Fig. 1

Amino acid sequences of exon 3 of the blue tit MHC-I, aligned with amino acid sequences of exon 3 of several other bird species: the chicken (Gallus gallus, Gaga BF*J3, accession number AY327148, alpha 2 region only, Livant et al. 2004), the Japanese quail (C. japonica, Coja, D29813Shiina et al. 1995), the duck (A. platyrhynchos, Anpl, AY294416, Mesa et al. 2004), the great reed warbler (A. arundinaceus, Acar cN20 exon 3 Westerdahl et al. 1999) and the Scarlet rosefinch (C. erythrinus, Caer U*01, FJ392762 Promerová et al. 2009), added from NCBI genbank. Asterisks mark the PBR while shaded areas mark, and numbers below the figure indicate the conserved sites as named by Kaufman et al. . The columns on the right indicate whether the alleles were found in cDNA and gDNA

Fig. 2

Phylogenetic tree for class I alleles in the blue tit. Numbers in the tree indicate the posterior probabilities expressed as a percentage (values below 50 not shown). The alleles of the allelic cluster with low diversity (group 1 supported by a posterior probability value of 100) are indicated by white dots, while all other alleles (group 2) have black dots. Abbreviations indicate from which population the DNA sample was taken (NL the Netherlands, SW Swedish, SP Spanish)

Fig. 3

RFLP gel of two blue tit families. The top row of numbers indicates individuals: M1 and F1 are parents of individuals 1–7 (M male, F female) and M2 and F2 are parents of individuals 8–13. The second row indicates the total number of bands present for each individual. A size standard in kilobase is shown on the right. The position of all RFLP bands found is indicated on the left of the gel. All RFLP bands were between 2.3 and 6.6 kb in length