Evolution of innate and adaptive immune genes in a non-model waterbird, the common tern

Minias, Piotr; Drzewińska‐Chańko, Joanna; Włodarczyk, Radosław

doi:10.1016/j.meegid.2021.105069

Cited by 6 publications

(5 citation statements)

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“…In our work, we aimed to compare the utility of different approaches in genotyping the MHC-DRB locus in species with a simple MHC system, such as the European roe deer, which has a single copy of the gene, and in red deer, which is a species with multiple DRB loci. Our results emphasise the need for a species-specific methodological approach, even when genotyping closely related mammalian species whose MHC genes might be quite complex but not as complex as in some other mammalian species (e.g., MHC class I in Iberian lynx [ 8 ] or other vertebrate taxa, such as birds [ 30 , 31 , 32 , 33 ]). Using multiple parallel methods in preliminary allele assessment offers the possibility to test which of the methods is the most appropriate for future genotyping projects, and it can also serve for validation of allele findings, as detecting an allele in a single individual with multiple approaches further supports its credibility.…”

Section: Discussionmentioning

confidence: 89%

Performance Comparison of Different Approaches in Genotyping MHC-DRB: The Contrast between Single-Locus and Multi-Locus Species

Svetličić

Konjević

Bužan

et al. 2022

Animals

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Major histocompatibility complex (MHC) genes are widely recognised as valuable markers for wildlife genetic studies given their extreme polymorphism and functional importance in fitness-related traits. Newly developed genotyping methods, which rely on the use of next-generation sequencing (NGS), are gradually replacing traditional cloning and Sanger sequencing methods in MHC genotyping studies. Allele calling in NGS methods remains challenging due to extreme polymorphism and locus multiplication in the MHC coupled with allele amplification bias and the generation of artificial sequences. In this study, we compared the performance of molecular cloning with Illumina and Ion Torrent NGS sequencing in MHC-DRB genotyping of single-locus species (roe deer) and species with multiple DRB loci (red deer) in an attempt to adopt a reliable and straightforward method that does not require complex bioinformatic analyses. Our results show that all methods work similarly well in roe deer, but we demonstrate non-consistency in results across methods in red deer. With Illumina sequencing, we detected a maximum number of alleles in 10 red deer individuals (42), while other methods were somewhat less accurate as they scored 69–81% of alleles detected with Illumina sequencing.

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Section: Discussionmentioning

confidence: 89%

Performance Comparison of Different Approaches in Genotyping MHC-DRB: The Contrast between Single-Locus and Multi-Locus Species

Svetličić

Konjević

Bužan

et al. 2022

Animals

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“…Nevertheless, our study is one of the few on non-model species that considers both molecular domains‒coded by exon 2 and exon 3 for MHC class I genes and coded by exon 2 for MHC class IIA and B genes‒making up the peptide-binding groove for both MHC classes. In doing so, we find that purported higher sequence polymorphism and signatures of positive selection in MHC-II compared to MHC-I in non-passerines [ 34 – 36 ] only holds when viewing half of the peptide binding groove (MHC-I exon 3 for class I and MHC-IIB exon 2 for class II). The evidence of stronger selection on class II than class I in non-passerines disappears when we can see the entire picture.…”

Section: Discussionmentioning

confidence: 90%

“…We found greater sequence divergence and stronger positive (diversifying) selection measured as number of positively selected sites and dN/dS at MHC-IIB exon 2 than MHC-I exon 3. Stronger measures of balancing selection for MHC-IIB exon 2 than MHC-I exon 3 were also found in other non-passerine species [ 34 – 36 ] and one explanation has been that different modes of selection act upon MHC-I and MHC-II depending on passerine or non-passerine status [ 34 , 68 ]. However, previous studies have compared only these two exons between the classes, essentially considering only half of the sequence encoding the peptide-binding groove.…”

Section: Discussionmentioning

confidence: 99%

“…For birds, there is accumulating evidence that life-history strategies that increase exposure to pathogen pressure are responsible for higher loci copy numbers [ 32 ] and stronger signatures of diversifying selection [ 33 ]. Recent studies have also shown that patterns of selection and sequence polymorphism in birds differ between MHC-I and MHC-II and speculate that these differences are also driven by relative selective pressure imposed by microparasites and macroparasites, respectively [ 34 – 36 ]. However, all the studies that support this hypothesis have only focused on MHC-I exon 3 and MHC-IIB exon 2, encoding only half of the class I and class II peptide-binding grooves.…”

Section: Introductionmentioning

confidence: 99%

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High functional allelic diversity and copy number in both MHC classes in the common buzzard

et al. 2023

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Background The major histocompatibility complex (MHC), which encodes molecules that recognize various pathogens and parasites and initiates the adaptive immune response in vertebrates, is renowned for its exceptional polymorphism and is a model of adaptive gene evolution. In birds, the number of MHC genes and sequence diversity varies greatly among taxa, believed due to evolutionary history and differential selection pressures. Earlier characterization studies and recent comparative studies suggest that non-passerine species have relatively few MHC gene copies compared to passerines. Additionally, comparative studies that have looked at partial MHC sequences have speculated that non-passerines have opposite patterns of selection on MHC class I (MHC-I) and class II (MHC-II) loci than passerines: namely, greater sequence diversity and signals of selection on MHC-II than MHC-I. However, new sequencing technology is revealing much greater MHC variation than previously expected while also facilitating full sequence variant detection directly from genomic data. Our study aims to take advantage of high-throughput sequencing methods to fully characterize both classes and domains of MHC of a non-passerine bird of prey, the common buzzard (Buteo buteo), to test predictions of MHC variation and differential selection on MHC classes. Results Using genetic, genomic, and transcriptomic high-throughput sequencing data, we established common buzzards have at least three loci that produce functional alleles at both MHC classes. In total, we characterize 91 alleles from 113 common buzzard chicks for MHC-I exon 3 and 41 alleles from 125 chicks for MHC-IIB exon 2. Among these alleles, we found greater sequence polymorphism and stronger diversifying selection at MHC-IIB exon 2 than MHC-I exon 3, suggesting differential selection pressures on MHC classes. However, upon further investigation of the entire peptide-binding groove by including genomic data from MHC-I exon 2 and MHC-IIA exon 2, this turned out to be false. MHC-I exon 2 was as polymorphic as MHC-IIB exon 2 and MHC-IIA exon 2 was essentially invariant. Thus, comparisons between MHC-I and MHC-II that included both domains of the peptide-binding groove showed no differences in polymorphism nor diversifying selection between the classes. Nevertheless, selection analysis indicates balancing selection has been acting on common buzzard MHC and phylogenetic inference revealed that trans-species polymorphism is present between common buzzards and species separated for over 33 million years for class I and class II. Conclusions We characterize and confirm the functionality of unexpectedly high copy number and allelic diversity in both MHC classes of a bird of prey. While balancing selection is acting on both classes, there is no evidence of differential selection pressure on MHC classes in common buzzards and this result may hold more generally once more data for understudied MHC exons becomes available.

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“…At the interspecific level, constraints in host and pathogen structure variation may lead to evolutionary convergence ( Walsh et al 2008 ; Świderská et al 2018 ; Těšický et al 2020 ), whereas TLR polymorphism at the intraspecific level may be maintained within populations via balancing selection. Though nonnegligible levels of functional, and potentially functional, variability at TLRs has recently been revealed across and within phylogenetically diverse vertebrate lineages, including humans ( Ferwerda et al 2007 ), domestic animals ( Leveque et al 2003 ; Świderská et al 2018 ), and wild species ( Alcaide and Edwards 2011 ; Quéméré et al 2015 ; Vinkler et al 2015 ; Minias et al 2021 ), the mechanisms of balancing selection actively maintaining this variation within populations are still debated.…”

Section: Toll-like Receptors—function Selection and Diversitymentioning

confidence: 99%

Selection Balancing at Innate Immune Genes: Adaptive Polymorphism Maintenance in Toll-Like Receptors

Minias

Vinkler

2022

Molecular Biology and Evolution

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Balancing selection is a classic mechanism for maintaining variability in immune genes involved in host-pathogen interactions. However, it remains unclear how widespread the mechanism is across immune genes other than the Major Histocompatibility Complex (MHC). While occasional reports suggest that balancing selection (heterozygote advantage, negative frequency-dependent selection and fluctuating selection) may act on other immune genes, current understanding of the phenomenon in non-MHC immune genes is far from solid. In this review, we focus on Toll-like receptors (TLRs), innate immune genes directly involved in pathogen recognition and immune response activation, as there is a growing body of research testing the assumptions of balancing selection in these genes. After reviewing infection- and fitness-based evidence, along with evidence based on population allelic frequencies and heterozygosity levels, we conclude that balancing selection maintains variation in TLRs, though it tends to occur under specific conditions in certain evolutionary lineages rather than being universal and ubiquitous. Our review also identifies key gaps in current knowledge and proposes promising areas for future research. Improving our understanding of host-pathogen interactions and balancing selection in innate immune genes is increasingly important, particularly regarding threats from emerging zoonotic diseases.

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Evolution of innate and adaptive immune genes in a non-model waterbird, the common tern

Cited by 6 publications

References 64 publications

Performance Comparison of Different Approaches in Genotyping MHC-DRB: The Contrast between Single-Locus and Multi-Locus Species

Performance Comparison of Different Approaches in Genotyping MHC-DRB: The Contrast between Single-Locus and Multi-Locus Species

High functional allelic diversity and copy number in both MHC classes in the common buzzard

Selection Balancing at Innate Immune Genes: Adaptive Polymorphism Maintenance in Toll-Like Receptors

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