Abstract

With a growing number of parasites and pathogens experiencing large-scale range expansions, monitoring diversity in immune genes of host populations has never been so important because it can inform on the adaptive potential to resist the invaders. Population surveys of immune genes are becoming common in many organisms, yet they are missing in the honey bee (Apis mellifera L.), a key managed pollinator species that has been severely affected by biological invasions. To fill the gap, here we identified single nucleotide polymorphisms (SNPs) in a wide range of honey bee immune genes and developed a medium-density assay targeting a subset of these genes. Using a discovery panel of 123 whole-genomes, representing seven A. mellifera subspecies and three evolutionary lineages, 180 immune genes were scanned for SNPs in exons, introns (< 4 bp from exons), 3’ and 5´UTR, and < 1 kb upstream of the transcription start site. After application of multiple filtering criteria and validation, the final medium-density assay combines 91 quality-proved functional SNPs marking 89 innate immune genes and these can be readily typed using the high-sample-throughput iPLEX MassARRAY system. This medium-density-SNP assay was applied to 156 samples from four countries and the admixture analysis clustered the samples according to their lineage and subspecies, suggesting that honey bee ancestry can be delineated from functional variation. In addition to allowing analysis of immunogenetic variation, this newly-developed SNP assay can be used for inferring genetic structure and admixture in the honey bee.

Highlights

  • The worldwide movements of humans and goods, coupled with climate change, have led to the introduction, and often successful spread, of many pathogens and parasites into novel environments, and this phenomenon is occurring at unprecedented temporal and spatial s­ cales[1]

  • In addition to be a vehicle for disseminating parasites and pathogens at the global scale, trade can help exotic gene flow within the A. mellifera natural range, leading to introgressive hybridization or even displacement of native ­subspecies[49,50,51]

  • We expanded the existing single nucleotide polymorphisms (SNPs)-tool box by developing a medium-density assay for screening polymorphisms in immune genes

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Summary

Introduction

The worldwide movements of humans and goods, coupled with climate change, have led to the introduction, and often successful spread, of many pathogens and parasites into novel environments, and this phenomenon is occurring at unprecedented temporal and spatial s­ cales[1]. The honey bee Apis mellifera L. has been impacted by introduced parasites and pathogens, most notably the mite Varroa destructor and the microsporidian Nosema ceranae[7,8,9,10] These are both native to Asia and have rapidly spread worldwide, after a host shift from Apis cerana to Apis mellifera[7,10]. The honey bee immune system is triggered when structural motifs on the surface of pathogens (pathogensassociated molecular patterns—PAMPs) bind to its receptors (pattern recognition receptors—PRRs) activating different pathways, depending on the pathogen. These pathways include Toll, IMD (immune deficiency), JakSTAT (Janus kinase and signal transducer and activator of transcription), and c-Jun N-terminal kinase (JNK). The link of these findings to inter-individual variability at the DNA level is lacking

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