Submitted to: PLoS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2012
Publication Date: 11/30/2012
Citation: Choi, M.Y., Vander Meer, R.K. 2012. Neuropeptide-mediated stimulation of pheromone biosynthesis in an ant. PLoS One. 7(11): e50400 1-8.
Interpretive Summary: Pheromones are well known to initiate behavioral or physiological responses in members of the same species. The chemistry and behaviors elicited by pheromones have advanced tremendously in the 50+ years since the first pheromone identification from the silkworm moth. However, the regulation of pheromone biosynthesis is not broadly understood. The red imported fire ant, S. invicta, is among the world’s 100 worst invasive alien species. In the United States this ant species infests more than 320 million acres in 13 southern tier states and Puerto Rico and are spreading northward. The behaviors and chemistry of several fire ant pheromones are well understood and extremely important to colony food procurement and social structure; however, regulation of pheromone production is unknown. Understanding this critical process could lead to novel control methods. Scientists from the Imported Fire Ant and Household Insect Unit at the Center for Medical, Agricultural and Veterinary Entomology, USDA, ARS, Gainesville, FL used a variety of techniques to address this difficult problem. Taken together, our results support the conclusion that a fire ant neuropeptide, SoiPBAN (Solenopsis invicta Pheromone Biosynthesis Activating Neuropeptide), stimulates recruitment pheromone biosynthesis in workers. We anticipate that the model presented here will lead to broader elucidation of PBAN’s role in insect pheromone biosynthesis. Regarding fire ants, the recruitment pheromone is one of many critical pheromones needed to maintain social structure. Our demonstration that the SoiPBAN receptor is expressed in other tissues including the head and poison gland, indicate that additional functions are yet to be elucidated.
Technical Abstract: Pheromones are well known to initiate behavioral or physiological responses in members of the same species. The chemistry and behaviors elicited by pheromones have advanced tremendously in the 50+ years since the first pheromone identification from the silkworm moth. However, the regulation of pheromone biosynthesis is not broadly understood. A significant breakthrough occurred in the late 1980s when a neuropeptide (Pheromone Biosynthesis Activating Neuropeptide, PBAN) was found to stimulate sex pheromone production in the female moth; however, in the ensuing decades demonstration of PBAN involvement in pheromone production was limited to additional moth sex pheromones. Here we show that PBAN stimulates production of the recruitment pheromone in the fire ant, Solenopsis invicta, suggesting broad applicability to insects, since all insects investigated have PBAN family peptides. Our conclusions are supported by the following: a) identification of the PBAN receptor from S. invicta, designated SoiPBAN-R; b) discovery that SoiPBAN-R is expressed in Dufour’s glands (DG), the source of the fire ant recruitment pheromone; c) injection of PBAN into workers stimulated recruitment pheromone production; d) RNA interference (RNAi) of SoiPBAN or SoiPBAN-R resulted in reduced recruitment pheromone levels in the DG. Many moth sex pheromones are biosynthesized in epithelial glands located in the last abdominal segments, usually with no lumen. This system lends itself to clear present or absent chemical analyses to demonstrate the effect of PBAN. However, pheromone stored in a lumen, e.g. DG of ants, is always present and is maintained within a range through biosynthetic activation and deactivation. This presents substantial impediments to measuring differences from hormonal stimulation. After decades of limited progress our results open the gates to a broader understanding of PBAN’s involvement in pheromone biosynthesis in Insecta.