100 million years of multigene family evolution: origin and evolution of the avian MHC class IIB

Abstract

Background: Gene duplication has led to a most remarkable adaptation involved in vertebrates' host-pathogen arms-race, the major histocompatibility complex (MHC). However, MHC duplication history is as yet poorly understood in non-mammalian vertebrates, including birds.

Results: Here, we provide evidence for the evolution of two ancient avian MHC class IIB (MHCIIB) lineages by a duplication event prior to the radiation of all extant birds >100 million years ago, and document the role of concerted evolution in eroding the footprints of the avian MHCIIB duplication history.

Conclusions: Our results suggest that eroded footprints of gene duplication histories may mimic birth-death evolution and that in the avian MHC the presence of the two lineages may have been masked by elevated rates of concerted evolution in several taxa. Through the presence of a range of intermediate evolutionary stages along the homogenizing process of concerted evolution, the avian MHCIIB provides a remarkable illustration of the erosion of multigene family duplication history.

Keywords: Birds; Birth-death evolution; Concerted evolution; Gene conversion; Gene duplication; Major histocompatibility complex; Recombination.

Fig. 1

a Schematic of the phylogenetic distribution of the avian DAB1 (green) and DAB2 (blue) MHCIIB lineages based on the phylogenetic placing of sequences (Fig. 2, Additional file 1) and on the screening of sequence signatures for DAB1- and DAB2-specific variants (panel b). The duplication event preceding the avian radiation is depicted by an asterisk. In parentheses, the number of species and sequences are provided for each order. Asterisks following parentheses indicate orders for which only one lineage was identified despite efforts to isolate the second lineage [28]. Accordingly, for orders with only a single lineage available on DNA databases obtained with non-significant sequencing efforts, branches are presented in dissolved colors. b Alignment of the 16 lineage-specific sites in exon 3. For each order, the most DAB1-like and the most DAB2-like sequence is presented. Dots in the alignment represent variants identical with the DAB1 sequence signature. Green and blue shading indicate variants identic with the DAB1-specific and DAB2-specific variants, respectively. Sites identified to trace duplication history using Saguaro are highlighted with hashes and red frames. c Degrees of divergence/homogenization of the lineages within avian orders. For each order, the number of pairwise differences between the most DAB1-like and the most DAB2-like sequences within the 16-bp signatures is provided. For orders with only one type of sequence, this number is zero and is indicated in grey where only a single sequence was available (usually from a genome assembly)

Fig. 2

Phylogenetic relationships of MHCIIB exon 3 sequences (first 220 bp). The two monophyletic clusters comprising sequences with predominantly DAB1 signature or DAB2 signature are shown in green and blue, respectively. Grey colored branches lead to sequences from pelecaniform and phoenicopteriform species with strongly intermingled lineage signatures. Sequence clusters with sequences from the same order have been collapsed for reasons of readability. A fully resolved topology is provided in Additional file 1. Symbols represent Bayesian posterior probabilities of the resolved-consensus tree: asterisks, ≥0.95; circles, 0.8–0.9; triangles, 0.5–0.8

Fig. 3

Intermingling of MHCIIB lineage-specific signatures by concerted evolution in pelecaniform and procellariiform birds. Green shading and dots in the alignment indicate identity with the DAB1 signature. Blue shading indicates identity with the DAB2 signature