Abstract
The evolution of advanced sociality in bees is associated with apparent modifications in juvenile hormone (JH) signaling. By contrast to most insects in which JH is a gonadotropin regulating female fertility, in the highly eusocial honey bee (Apis mellifera) JH has lost its gonadotrophic function in adult females, and instead regulates age-related division of labor among worker bees. In order to shed light on the evolution of JH signaling in bees we performed allatectomy and replacement therapies to manipulate JH levels in workers of the "primitively eusocial" bumblebee Bombus terrestris. Allatectomized worker bees showed remarkable reduction in ovarian development, egg laying, Vitellogenin and Krüppel homolog 1 fat body transcript levels, hemolymph Vitellogenin protein abundance, wax secretion, and egg-cell construction. These effects were reverted, at least partially, by treating allatectomized bees with JH-III, the natural JH of bees. Allatectomy also affected the amount of ester component in Dufour's gland secretion, which is thought to convey a social signal relating to worker fertility. These findings provide a strong support for the hypothesis that in contrast to honey bees, JH is a gonadotropin in bumblebees and lend credence to the hypothesis that the evolution of advanced eusociality in honey bees was associated with major modifications in JH signaling.
Highlights
Endocrine systems typically integrate multiple environmental signals and coordinate processes in multiple tissues
Our results show that juvenile hormone (JH) is necessary for oocyte development and maturation and is involved in the regulation of vitellogenesis and several additional physiological processes that are associated with reproduction
Our results show that JH is necessary for oocyte development and egg-laying in B. terrestris workers and provide the strongest available support for the hypothesis that JH functions as a gonadotropin in the bumblebee B. terrestris
Summary
Endocrine systems typically integrate multiple environmental signals and coordinate processes in multiple tissues. Even limited modifications in endocrine signaling pathways may affect multiple tissues and produce profound coordinated changes in morphology, physiology, or function. These characteristics make endocrine systems good candidates for accounting for extensive evolutionary novelties such as those associated with the evolution of animal societies [1]. Consistent with this premise, there is evidence implicating hormones in the regulation of processes such as caste differentiation and division of labor that are pivotal for the organization of insect societies (reviewed in [2]). While most bee species are solitary, there are many social species that exhibit diverse levels of social complexity, from small groups consisting of only a handful of individuals, to the perennial societies of honey bees and stingless bees with their complex communication systems, morphological caste system, and intricate division of labor among workers [3,4]
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