Characterization of MHC class I in a long distance migratory wader, the Icelandic black-tailed godwit

Abstract

The major histocompatibility complex (MHC) encodes proteins that are central for antigen presentation and pathogen elimination. MHC class I (MHC-I) genes have attracted a great deal of interest among researchers in ecology and evolution and have been partly characterized in a wide range of bird species. So far, the main focus has been on species within the bird orders Galliformes and Passeriformes, while Charadriiformes remain vastly underrepresented with only two species studied to date. These two Charadriiformes species exhibit striking differences in MHC-I characteristics and MHC-I diversity. We therefore set out to study a third species within Charadriiformes, the Icelandic subspecies of black-tailed godwits (Limosa limosa islandica). This subspecies is normally confined to parasite-poor environments, and we hence expected low MHC diversity. MHC-I was partially characterized first using Sanger sequencing and then using high-throughput sequencing (MiSeq) in 84 individuals. We verified 47 nucleotide alleles in open reading frame with classical MHC-I characteristics, and each individual godwit had two to seven putatively classical MHC alleles. However, in contrast to previous MHC-I data within Charadriiformes, we did not find any evidence of alleles with low sequence diversity, believed to represent non-classical MHC genes. The diversity and divergence of the godwits MHC-I genes to a large extent fell between the previous estimates within Charadriiformes. However, the MHC genes of the migratory godwits had few sites subject to positive selection, and one possible explanation could be a low exposure to pathogens.Electronic supplementary materialThe online version of this article (doi:10.1007/s00251-017-0993-7) contains supplementary material, which is available to authorized users.

Allelic diversity and patterns of selection at the major histocompatibility complex class I and II loci in a threatened shorebird, the Snowy Plover (Charadrius nivosus)

“…Consistent with this, we found that sites with signatures of purifying selection were predominantly non-PBR sites, whereas five of the six sites under diversifying selection in the MHC class I and in one site at MHC class II corresponded to PBR sites. Similar patterns were observed in another shorebird, the Icelandic Black-tailed Godwit [26], and shown in a recent comparative study of selection at the avian MHC [42].…”

“…The order Charadriiformes does not seem to fit to this proposed rule. Consistent with Minias et al [42], gulls and most of the alcids show a strong signature of selection at MHC class II and weaker selection at MHC class I, but the paraphyletic group of shorebirds (plovers and sandpipers) instead shows a pattern more similar to passerines [16,25,26,28,29,44]. Several morphological or ecological variables may explain this discrepancy.…”

“…The low genetic diversity may be a common feature of island populations that are thought to be exposed to fewer pathogens than continental pathogens [55]. For example, among shorebirds, Icelandic Black-tailed Godwits did not show positive selection at MHC class I PBR sites [26]. Other biogeographic features could contribute to the observed differences in genetic diversity.…”

“…In contrast, in Passeriformes, the MHC shows a complex architecture, and is frequently composed of multiple expressed loci and pseudogenes [1,23,24]. Other groups of birds, such as the Charadriiformes, appear to have a diversity and complexity intermediate between chicken and Passeriformes [25,26]. The differences in the number and organization of the MHC genes in vertebrates might be best explained by different evolutionary dynamics in the birth and death of genes [27].…”

“…Within the order Charadriiformes, study of the MHC have so far been restricted to three families: Alcidae, Laridae and Scolopacidae. These studies revealed considerable differences in the diversity and organization of the Charadriiform MHC [16,25,26,28,29]. To investigate which mechanisms generate and promote MHC evolution and diversity [9], studies in more phylogenetically distinct families are required.…”