Abstract
BackgroundRegulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 (Kr-h1), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera.ResultsIn contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders.ConclusionsOur results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.
Highlights
Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood
Brain Krüppel homolog 1 (Kr-h1) levels were significantly lower in queenright workers in the second and third trial (t(24) = -2.64, P = 0.014 and t(24) = -3.68, P = 0.001 respectively; Fig. 1A); a similar, but statistically not significant trend was obtained in the first trial (t(22) = -1.92; P = 0.068)
Our results suggest that Kr-h1 is associated with juvenile hormone (JH) mediated regulation of reproduction in bumble bees
Summary
Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Hereafter referred to as "social pathways", presumably link social signals from the queen and other workers with alterations in worker physiology, which in turn lead to changes in behavioral state (e.g. worker task) that are integrated into an emerging colony level function. These social pathways need to include sensory and integrative systems that ensure that the individual is tuned to the relevant social signals, as well as neuroendocrine signaling systems that integrate the molecular and physiological processes needed for producing the appropriate social behavior. Allelic differences at the Gp-9 locus in fire ants are associated with differences in colony structure, but the number of linked genes in this locus and their molecular functions are not known [11]
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