New data from basal Australian songbird lineages show that complex structure of MHC class II β genes has early evolutionary origins within passerines

Abstract

Background: The major histocompatibility complex (MHC) plays a crucial role in the adaptive immune system and has been extensively studied across vertebrate taxa. Although the function of MHC genes appears to be conserved across taxa, there is great variation in the number and organisation of these genes. Among avian species, for instance, there are notable differences in MHC structure between passerine and non-passerine lineages: passerines typically have a high number of highly polymorphic MHC paralogs whereas non-passerines have fewer loci and lower levels of polymorphism. Although the occurrence of highly polymorphic MHC paralogs in passerines is well documented, their evolutionary origins are relatively unexplored. The majority of studies have focussed on the more derived passerine lineages and there is very little empirical information on the diversity of the MHC in basal passerine lineages. We undertook a study of MHC diversity and evolutionary relationships across seven species from four families (Climacteridae, Maluridae, Pardalotidae, Meliphagidae) that comprise a prominent component of the basal passerine lineages. We aimed to determine if highly polymorphic MHC paralogs have an early evolutionary origin within passerines or are a more derived feature of the infraorder Passerida.

Results: We identified 177 alleles of the MHC class II β exon 2 in seven basal passerine species, with variation in numbers of alleles across individuals and species. Overall, we found evidence of multiple gene loci, pseudoalleles, trans-species polymorphism and high allelic diversity in these basal lineages. Phylogenetic reconstruction of avian lineages based on MHC class II β exon 2 sequences strongly supported the monophyletic grouping of basal and derived passerine species.

Conclusions: Our study provides evidence of a large number of highly polymorphic MHC paralogs in seven basal passerine species, with strong similarities to the MHC described in more derived passerine lineages rather than the simpler MHC in non-passerine lineages. These findings indicate an early evolutionary origin of highly polymorphic MHC paralogs in passerines and shed light on the evolutionary forces shaping the avian MHC.

Keywords: Accordion model; Birth-and-death model; Concerted evolution; Convergent evolution; Corvida; Gene duplication; Passerida; Trans-species polymorphism.

Fig. 1

Relationships among major passerine families. Grey shading indicates families included in this study and asterisks denote families in the Corvida that have been previously studied. Phylogeny constructed using the Ericson backbone in birdtree.org [72] and rooted with Gallus gallus

Fig. 2

Relationships of MHC class II β exon 2 sequences among basal passerine species. a Bayesian phylogeny of MHC alleles from the seven basal passerine species in this study, rooted with Crocodylus niloticus; asterisks denote major branches with posterior probabilities > 90 %, and pseudoalleles are indicated by arrows. b Neighbour-net of MHC class II β exon 2 sequences from seven basal passerine species. Sequences are colour coded by family

Fig. 3

Basal passerine MHC class II β exon 2 sequences in the wider avian context. Bayesian phylogeny of MHC alleles from passerine and non-passerine families, rooted with Crocodylus niloticus. Asterisks denote major branches with posterior probabilities > 90 % and filled circles denote passerine species from the Corvida. Group A contains the majority of sequences from honeyeaters, pardalotes and fairy-wrens. Group B contains the remaining 18 sequences from these species, which comprise nine pseudoalleles and nine sequences with aspartic acid (D) or alanine (A) instead of glutamic acid (E) in the first position (see Additional file 4)