Abstract

Queen pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, queen pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged >150MYA and evolved queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to queen pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how queen pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor.

Highlights

  • Queen pheromones are chemical signals that mediate reproductive division of labor in eusocial animals

  • Many genes showed statistically significant differential expression between the pheromone-treated and control groups in A. mellifera (322 genes), L. flavus (290), and L. niger (135), and a single gene was significant in B. terrestris (Fig. 1a; Supplementary Tables 2–5)

  • If our average power to detect a pheromone-sensitive gene in one species were 40%, we would only detect about 0.44 = 2.6% of genes that were pheromone sensitive in all four species

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Summary

Introduction

Queen pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Queen pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged >150MYA and evolved queens and workers independently. We measure the transcriptomic consequences of experimental exposure to queen pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Our results reveal how queen pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor. Ants and wasps evolved eusociality (and queen-worker communication) independently[13], most Hymenopteran queen pheromones are thought to be composed of chemically similar compounds[1,2]. The Apis research bears repeating because only 18 of c. 1000 differentially expressed genes from the first study replicated in the second (three-fold fewer genes replicated than expected by chance alone[16])

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