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Characterization of MHC class I and II genes in a subantarctic seabird, the blue petrel, Halobaena caerulea (Procellariiformes)

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Abstract

The great polymorphism observed in the major histocompatibility complex (MHC) genes is thought to be maintained by pathogen-mediated selection possibly combined with MHC-disassortative mating, guided by MHC-determined olfactory cues. Here, we partly characterize the MHC class I and II B of the blue petrel, Halobaena caerulea (Procellariiformes), a bird with significant olfactory abilities that lives under presumably low pathogen burdens in Subantarctica. Blue petrels are long-lived, monogamous birds which suggest the necessity of an accurate mate choice process. The species is ancestral to songbirds (Passeriformes; many MHC loci), although not to gamefowls (Galliformes; few MHC loci). Considering the phylogenetic relationships and the low subantarctic pathogen burden, we expected few rather than many MHC loci in the blue petrel. However, when we analysed partial MHC class I and class II B cDNA and gDNA sequences we found evidence for as many as at least eight MHC class I loci and at least two class II B loci. These class I and II B sequences showed classical MHC characteristics, e.g. high nucleotide diversity, especially in putative peptide-binding regions where signatures of positive selection was detected. Trans-species polymorphism was found between MHC class II B sequences of the blue petrel and those of thin-billed prion, Pachyptila belcheri, two species that diverged ∼25 MYA. The observed MHC allele richness in the blue petrel may well serve as a basis for mate choice, especially since olfactory discrimination of MHC types may be possible in this species.

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Acknowledgements

This work was supported by the Institut Polaire Francais Paul-Emile Victor (IPEV programme ETHOTAAF no. 354 to FB), and the Agence Nationale de la Recherche Francaise (AMBO ANR-08-BLAN-0117-01 to FB). All aspects of the study were performed according to guidelines established by the IPEV and the CNRS for the ethical treatment of animals and complied with current French regulations. We are grateful to Jerome Mardon, Aurore Malapert and all the field workers who helped through the programme ETHOTAAF over the years. Many thanks to Marie-Pierre Dubois at CEFE, Montpellier and the ecological MHC group in Lund.

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  1. Maria Strandh

    Present address: Molecular Ecology and Evolution Lab, Lund university, Ecology building, 223 62, Lund, Sweden

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  1. Behavioral Ecology Group, CEFE-CNRS, 1919 Route de Mende, 34293, Montpellier Cedex 5, France

    Maria Strandh & Francesco Bonadonna

  2. Molecular Ecology and Evolution Lab, Lund university, Ecology building, 223 62, Lund, Sweden

    Mimi Lannefors & Helena Westerdahl

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Supplementary Fig. 1

Phylogenetic tree of major histocompatibility complex class I exons 2–4 translated sequences (Haca-UA*xxL, GenBank accession numbers, Acc nr JF276877–JF276884) from the blue petrel, Halobaena caerulea, five other bird species (Acc nr and species codes are given: Grca Grus canadensis pratensis, Anan Anser anser, Anpl Anas platyrhynchos, Gaga Gallus gallus and Acar Acrocephalus arundinaceus). Human HLA-A (Hosa_NM002116) was used as outgroup. Neighbour-joining bootstrap consensus tree from 2,000 replicates (Felsenstein 1985; Saitou and Nei 1987) constructed in MEGA4 (Tamura et al. 2007). Filled squares/circles represent sequences from each of two blue petrel individuals (PDF 386 kb)

Supplementary Fig. 2

Amino acid alignment of major histocompatibility complex class I exon 3 translated sequences (Haca-UA*01-Haca-UA*45, Acc nr JF276832–JF276876) from the blue petrel, Halobaena caerulea, five other bird species (Acc nr and species codes are given: Grca Grus canadensis pratensis, Anan Anser anser, Anpl Anas platyrhynchos, Gaga Gallus gallus, Acar Acrocephalus arundinaceus) and human HLA-A (Hosa_NM002116). Peptide-binding regions were inferred (a pocket a, f pocket f, c other peptide contacts, t t-cell contacts) (Wallny et al. 2006). Positively selected amino acid sites (plus sign) identified with model 8 in CODEML, PAML (Yang 2007) (PDF 33 kb)

Supplementary Fig. 3

Southern blots of major histocompatibility complex (MHC) probes hybridized to Pvu II cleaved genomic DNA from four individuals of blue petrels, Halobaena caerulea. Each lane represents an individual (1–4). The left panel shows a MHC class I exon 3 probed blot and the right panel a MHC class II B exon 2 probed blot of the same four individuals (PDF 323 kb)

Supplementary Fig. 4

Amino acid alignment of major histocompatibility complex class II B exon 2 translated sequences (Haca-DAB*01-Haca-DAB*08, Acc nr JF276885–JF276892) from the blue petrel, Halobaena caerulea, and the thin-billed prion, Pachyptila belcheri (Pabe, Acc nr are given). Peptide-binding regions were inferred (c peptide contacts) (Brown et al. 1993). Positively selected amino acid sites (plus sign) identified with model 8 in CODEML, PAML (Yang 2007) (PDF 31 kb)

Supplementary Table 1

Major histocompatibility alleles (class I Haca-UA, class II B Haca-DAB, L long sequences, GenBank Acc nr JF276832–JF276894) identified by sequencing MHC clones from 25 blue petrel, Halobaena caerulea, individuals (1–25; g genomic DNA, c cDNA) (DOC 157 kb)

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Strandh, M., Lannefors, M., Bonadonna, F. et al. Characterization of MHC class I and II genes in a subantarctic seabird, the blue petrel, Halobaena caerulea (Procellariiformes). Immunogenetics 63, 653–666 (2011). https://doi.org/10.1007/s00251-011-0534-8

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