Juvenile hormone signaling and the evolution of advanced eusociality in bees
Guy Bloch (The Hebrew University of Jerysalem, Israel)
Juvenile hormone (JH) is the ancient gonadotropin of insects but not for advanced eusocial honey bees, where it regulates division of labor. To probe the evolutionary basis of this change, we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH- regulated processes in a “primitively eusocial” bumble bee, where JH is the major gonadotropin. We show that JH influences behavior such as dominance, aggression and circadian rhythmicity, but not task performance (i.e., division of labor). Our transcriptomic analyses show that in the fat body, more JH-regulated genes were upregulated and enriched for metabolic and biosynthetic pathways. Remarkably, in the brain, most JH-regulated genes were downregulated and enriched for protein turnover pathways, suggesting an encdocrine-mediated tradeoff. Supporting this possibility, brain ribosomal protein gene expression was downregulated in dominant workers, which naturally have high JH titers, but not in hormone-treated honey bees. These findings suggest that the evolution of advanced eusociality was associated with modifications in hormonal signaling supporting extended and extremely high fertility while reducing the ancient costs of high gonadotropin titers to the brain. Thus, our findings link two remarkable physiological traits of advanced eusocial insects: first, they defy the widespread trade-off between reproduction and longevity, second, JH, which is the ancient insect gonadotropin, does not appear to regulate fertility in some social insects such as honey bees and some ants. Our findings suggest that these two traits are linked because high JH titres would have caused a serious cost to queens that are highly fertile over extended periods, and therefore the evolution of eusociality in these lineages was associated with modifications in JH signalling pathways.