Immune pathways and defence mechanisms in honey bees Apis mellifera

Abstract

Social insects are able to mount both group-level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome-wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one-third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.

Figure 1

Candidate honey bee members for the Toll pathway. Names are given for the Drosophila pathway components, along with vertebrate orthologues (in parentheses). Honey bee matches given as named during the genome project. Honey bee names in italics refer to genes with close paralogues which cannot readily be distinguished with respect to pathway components from Drosophila. Underlining indicates genes shown to be transcriptionally up-regulated after immune challenge.

Figure 2

Candidate honey bee members for the Imd, JNK and JAK/STAT pathways, below names for Drosophila pathway components along with vertebrate orthologues (in parentheses). Honey bee matches presented as named during the genome project. Honey bee names in italics refer to genes with close paralogues which cannot readily be distinguished with respect to pathway components from Drosophila. Underlining indicates genes shown to be transcriptionally up-regulated after immune challenge.

Figure 3

Transcript abundances for immune candidate genes in adult workers 24 h after injections of Escherichia coli (Ec), saline buffer, or the bee pathogen Paenibacillus larvae, and controls (left four columns). Two columns on right show transcript abundances in 2nd-instar larvae challenged orally with an infective dose of P. larvae or unchallenged controls. Cluster A = genes strongly up-regulated by adult injection or wounding, Cluster B = genes up-regulated in infected larvae, Cluster C = genes down-regulated or minimally changed in challenged bees.

Figure 4

(A) Phylogenetic relationships estimated for peptidoglycan recognition protein (PGRP) family members for honey bees (underlined), Drosophila melanogaster (Dm), and Anopheles gambiae (Ag). Circles indicate apparent three-way orthologues for these three species. (B) Relationships between members of the Class B scavenger receptors, including the above insect members as well as mouse and human CD36 proteins. (C) Relationships between honey bee serine proteases (AmelSP) and serine-protease homologues (AmelSPH) and a representative subset of those from Drosophila melanogaster and Manduca sexta (Ms). (D) Phylogenetic relationships of honey bee serpins (AmelSpn) compared to homologues in Dm, Ag and Ms, colours as above. (E) Toll and Toll-like receptors for honey bees, Dm, Ag, Bombyx mori (Bm) and Aedes aegypti (Ae). Relationships derived by neighbor joining as described in the text.