Abstract
Simple SummaryIn diverse animal species, individuals establish dominance hierarchies by means of agonistic interactions. Dominance rank is functionally significant because it affects access to vital resources such as mates, food, and shelter, but little is known on the underlying genetic and molecular mechanisms, specifically in insects, and among females. We tested the hypothesis that Krüppel homologue 1, a key endocrine signaling gene, influences dominance among bumble bee female workers. We developed and validated a new nanoparticle-based protocol to down-regulate gene expression in bumble bees. Using this protocol, we show that Krüppel homologue 1 mediates endocrine influences, not only on fertility and wax production, but also on aggression and dominance rank. These findings, which establish the first causal link between a gene and a dominance rank in a social insect, are important for determining whether there are general molecular principles governing dominance ranks across gender and animal species.Dominance hierarchies are ubiquitous in invertebrates and vertebrates, but little is known on how genes influence dominance rank. Our gaps in knowledge are specifically significant concerning female hierarchies, particularly in insects. To start filling these gaps, we studied the social bumble bee Bombus terrestris, in which social hierarchies among females are common and functionally significant. Dominance rank in this bee is influenced by multiple factors, including juvenile hormone (JH) that is a major gonadotropin in this species. We tested the hypothesis that the JH responsive transcription factor Krüppel homologue 1 (Kr-h1) mediates hormonal influences on dominance behavior. We first developed and validated a perfluorocarbon nanoparticles-based RNA interference protocol for knocking down Kr-h1 expression. We then used this procedure to show that Kr-h1 mediates the influence of JH, not only on oogenesis and wax production, but also on aggression and dominance rank. To the best of our knowledge, this is the first study causally linking a gene to dominance rank in social insects, and one of only a few such studies on insects or on female hierarchies. These findings are important for determining whether there are general molecular principles governing dominance rank across gender and taxa.
Highlights
Social hierarchies are ubiquitous in invertebrates and vertebrates
Compared to handling control bees and those injected with pG double strand RNA (dsRNA), the bees injected with naked Krüppel homologue 1 (Kr-h1) dsRNA showed fewer threatening displays when observed at three, but not at six hours, after the second injection (Supplementary Figure S3F; Kruskal–Wallis test, χ2(threatening display, 3 after) = 9.93, df = 2, p = 0.007; χ2(threatening display, 6 after) = 0.34, df = 2, p = 0.843, respectively)
By showing that bees with reduced Kr-h1 transcript abundance show less dominance behavior and have a lower dominance rank compared to bees injected with control dsRNA, we establish for the first time a causal link between a specific gene and dominance rank in a social insect in which dominance hierarchies are established between females
Summary
Social hierarchies are ubiquitous in invertebrates and vertebrates. Behavioral dominance is the basic principle organizing social hierarchies and is typically established by the outcome of multiple contests between pairs of conspecifics which are resolved with a clear dominance rank. Prior experience (e.g., winner, loser, or bystander effects; chronological age; fighting experience), and the subjective evaluation of a resource, including motivation, may be crucial, adding additional levels of complexity [13,14] It is not obvious how such group-level, context-dependent traits can be genetically inherited [10]. In spite of these difficulties, artificial selection in laboratory studies with various species including rodents [15,16] and insects [17], have shown that dominance rank can be selected, lending credence to the notion that social rank is influenced by genes. Little is known of the identity of specific genes underlying the expression of dominance behavior and the mechanisms by which they influence dominance rank [9]
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