The evolution of extreme fertility defied ancestral gonadotropin mediated brain-reproduction tradeoff

Gonadotropic hormones coordinate processes in diverse tissues regulating animal reproductive physiology and behavior. Juvenile hormone (JH) is the ancient and most common gonadotropin in insects, but not in advanced eusocial honey bees and ants. To probe the evolutionary basis of this change, we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH regulated processes in a bumble bee showing an intermediate level of sociliality. We found that in the fat body, more JH-regulated genes were upregulated and enriched for metabolic and biosynthetic pathways. This transcriptomic pattern is consistent with earlier evidence that JH is the major gonadotropin in the bumble bee. In the brain, most JH-regulated genes were downregulated and enriched for protein turnover pathways. Brain ribosomal protein gene expression was similarly downregulated in dominant workers, which naturally have high JH titers. In other species, similar downregulation of protein turnover is found in aging brains or under stress, and is associated with compromised long-term memory and health. These findings suggest a previously unknown gonadotropin-mediated tradeoff. We did not find a similar downregulation of protein turnover pathways in the brain of honey bees in which JH is not a gonadotropin but rather regulates division of labor. These differences between JH effets in the bumble bee and in the advanced eusocial honey bee 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.