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

ABSTRACT: 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.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.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.

SUBMITTER: Goebel J

PROVIDER: S-EPMC5470263 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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

Goebel Julien J Promerová Marta M Bonadonna Francesco F McCoy Karen D KD Serbielle Céline C Strandh Maria M Yannic Glenn G Burri Reto R Fumagalli Luca L

BMC genomics 20170613 1

<h4>Background</h4>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.<h4>Results</h4>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 rol ...[more]

PMID: 28610613

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Project description:Host-pathogen interactions are a major evolutionary force promoting local adaptation. Genes of the major histocompatibility complex (MHC) represent unique candidates to investigate evolutionary processes driving local adaptation to parasite communities. The present study aimed at identifying the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of European minnows (Phoxinus phoxinus). To this end, we isolated and genotyped exon 2 of two MHCIIB gene duplicates (DAB1 and DAB3) and 1'665 amplified fragment length polymorphism (AFLP) markers in nine populations, and characterized local bacterial communities by 16S rDNA barcoding using 454 amplicon sequencing. Both MHCIIB loci exhibited signs of historical balancing selection. Whereas genetic differentiation exceeded that of neutral markers at both loci, the populations' genetic diversities were positively correlated with local pathogen diversities only at DAB3. Overall, our results suggest pathogen-mediated local adaptation in European minnows at both MHCIIB loci. While at DAB1 selection appears to favor different alleles among populations, this is only partially the case in DAB3, which appears to be locally adapted to pathogen communities in terms of genetic diversity. These results provide new insights into the importance of host-pathogen interactions in driving local adaptation in the European minnow, and highlight that the importance of adaptive processes driving MHCIIB gene evolution may differ among duplicates within species, presumably as a consequence of alternative selective regimes or different genomic context. Using next-generation sequencing, the present manuscript identifies the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of a cyprinid fish: the European minnow (Phoxinus phoxinus). We highlight that the relative importance of neutral versus adaptive processes in shaping immune competence may differ between duplicates as a consequence of alternative selective regimes or different genomic contexts.

Project description:Large-scale adaptive radiations might explain the runaway success of a minority of extant vertebrate clades. This hypothesis predicts, among other things, rapid rates of morphological evolution during the early history of major groups, as lineages invade disparate ecological niches. However, few studies of adaptive radiation have included deep time data, so the links between extant diversity and major extinct radiations are unclear. The intensively studied Mesozoic dinosaur record provides a model system for such investigation, representing an ecologically diverse group that dominated terrestrial ecosystems for 170 million years. Furthermore, with 10,000 species, extant dinosaurs (birds) are the most speciose living tetrapod clade. We assembled composite trees of 614-622 Mesozoic dinosaurs/birds, and a comprehensive body mass dataset using the scaling relationship of limb bone robustness. Maximum-likelihood modelling and the node height test reveal rapid evolutionary rates and a predominance of rapid shifts among size classes in early (Triassic) dinosaurs. This indicates an early burst niche-filling pattern and contrasts with previous studies that favoured gradualistic rates. Subsequently, rates declined in most lineages, which rarely exploited new ecological niches. However, feathered maniraptoran dinosaurs (including Mesozoic birds) sustained rapid evolution from at least the Middle Jurassic, suggesting that these taxa evaded the effects of niche saturation. This indicates that a long evolutionary history of continuing ecological innovation paved the way for a second great radiation of dinosaurs, in birds. We therefore demonstrate links between the predominantly extinct deep time adaptive radiation of non-avian dinosaurs and the phenomenal diversification of birds, via continuing rapid rates of evolution along the phylogenetic stem lineage. This raises the possibility that the uneven distribution of biodiversity results not just from large-scale extrapolation of the process of adaptive radiation in a few extant clades, but also from the maintenance of evolvability on vast time scales across the history of life, in key lineages.

Dataset Information

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

Publications

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

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