Characterization of class II β chain major histocompatibility complex genes in a family of Hawaiian honeycreepers: ‘amakihi (Hemignathus virens)

Abstract

Hawaiian honeycreepers (Drepanidinae) have evolved in the absence of mosquitoes for over five million years. Through human activity, mosquitoes were introduced to the Hawaiian archipelago less than 200 years ago. Mosquito-vectored diseases such as avian malaria caused by Plasmodium relictum and Avipoxviruses have greatly impacted these vulnerable species. Susceptibility to these diseases is variable among and within species. Due to their function in adaptive immunity, the role of major histocompatibility complex genes (Mhc) in disease susceptibility is under investigation. In this study, we evaluate gene organization and levels of diversity of Mhc class II β chain genes (exon 2) in a captive-reared family of Hawaii 'amakihi (Hemignathus virens). A total of 233 sequences (173 bp) were obtained by PCR+1 amplification and cloning, and 5720 sequences were generated by Roche 454 pyrosequencing. We report a total of 17 alleles originating from a minimum of 14 distinct loci. We detected three linkage groups that appear to represent three distinct haplotypes. Phylogenetic analysis revealed one variable cluster resembling classical Mhc sequences (DAB) and one highly conserved, low variability cluster resembling non-classical Mhc sequences (DBB). High net evolutionary divergence values between DAB and DBB resemble that seen between chicken BLB system and YLB system genes. High amino acid identity among non-classical alleles from 12 species of passerines (DBB) and four species of Galliformes (YLB) was found, suggesting that these non-classical passerine sequences may be related to the Galliforme YLB sequences.

Parallel evolution of gene classes, but not genes: Evidence from Hawai'ian honeycreeper populations exposed to avian malaria

“…Moreover, host MHC variation has been linked to disease outcome in a variety of vertebrate infectious diseases (e.g., Grimholt et al., ; Hawley & Fleischer, ; Kaufman, ; Tarleton, Grusby, Postan, & Climcher, ; Turner, McAllister, Xu, & Tapping, ; Savage & Zamudio, 2011), and avian malaria in passerines in particular (Bonneaud, Pérez‐Tris, Federici, Chastel, & Sorci, ; Westerdahl et al., ). Therefore, the fact that our genomewide SNP assay recovered MHC as associated with malaria‐induced selection is consistent with other patterns of selection on MHC observed in honeycreepers (Jarvi, Tarr, Mcintosh, Atkinson, & Fleischer, ; Jarvi et al., ).…”

Coloniality and migration are related to selection on MHC genes in birds

“…Also, the utility of dN/dS ratios to detect balancing selection depends on the degree of polymorphism within species, as saturation of synonymous sites may lead to biased dN/dS estimations in highly divergent allelic lineages (Castric and Vekemans 2007;Fijarczyk and Babik 2015). Thus, these limitations should be openly acknowledged and further tested, as nucleotide substitution rates remain among the most popular measures of balancing selection acting on MHC genes, even at the level of a single species or population (e.g., Knafler et al 2014;Bracamonte et al 2015;Eimes et al 2015;Jaeger et al 2016;Jarvi et al 2016).…”

Avian MHC Evolution in the Era of Genomics: Phase 1.0

“…The first generation of high-throughput MHC studies has revealed remarkably high levels of MHC diversity in many bird species [40,87,88,89,90,91,92], especially among passerine birds (Passeriformes). Despite early evidence from traditional MHC genotyping techniques that MHC diversity was higher in passerine than in non-passerine clades [24,93,94,95,96,97], the extreme levels of MHC diversity detected with high-throughput sequencing in some passerines was unprecedented and unexpected.…”

“…The high MHC polymorphism and the associations between MHC genes and fitness measures have led to interest in these genes from a conservation perspective, and it has been suggested that measures to maintain or promote MHC diversity should play a role in conservation efforts in endangered species [131,132,133,134,135]. Birds are no exception, with a number of studies on endangered or near threatened species, such as Hawaiian honeycreepers ( Drepanidinae ), New Zealand black robins ( Petroica traversi ), Seychelles warblers ( Acrocephalus sechellensis ), and crested ibis, focusing on MHC gene diversity [89,95,136,137].…”