Biogenic amines shift during the pre-reproductive to reproductive transition in the small carpenter bee, Ceratina calcarata
The shift from solitary to social living is a major evolutionary transition for social insects. In bees, this transition is marked by certain females becoming reproductive and reducing their role in nest and offspring care, duties that are assumed by other females. Biogenic amines play a significant role in regulating these behaviors in both solitary and social insects. How has the function of biogenic amines in solitary insects been coopted for social behaviors? Here, we used Ceratina calcarata, a behaviorally well-studied small subsocial carpenter bee to explore how biogenic amines may play a role in the reproductive shift over a season. We found that as females transition from a pre-reproductive to reproductive state, ovarian development is accompanied by an increase in brain levels of octopamine and serotonin. For comparison, we provide the first characterization of biogenic amines in the brains of males. These results suggest the essential role of biogenic amines in the transition of reproductive states in a bee on the brink of sociality and provide a deeper understanding of how biogenic amines may have influenced the evolution of social behavior.
Keywordsbiogenic amines reproductive status octopamine serotonin incipiently social
We thank Salena Helmreich, Wyatt Shell, and Jacob Withee for assistance with nest collections.
CNC, SPL, and SMR conceived the research experiment, collected, and analyzed data and contributed to manuscript preparation. CSB assisted with data interpretation and manuscript preparation. All authors read and approved the final manuscript.
This work was supported by funding from the University of New Hampshire to SMR, National Science Foundation—Integrative Organismal Systems: Behavioral Systems (1456296) to SMR and National Science Foundation Postdoctoral Research Fellowship (1523664) to SPL. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no potential conflict of interest in relation to the study in this paper.
- Barron, A. B., Maleszka, R., Meer, R. K. Vander and Robinson, G. E. (2007). Octopamine modulates honey bee dance behavior. Sci. York 104, 1703–1707.Google Scholar
- Brent, C. S., Miyasaki, K., Vuong, C., Miranda, B., Steele, B., Brent, K. G. and Nath, R. (2016). Regulatory roles of biogenic amines and juvenile hormone in the reproductive behavior of the western tarnished plant bug (Lygus hesperus). J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 186, 169–179.CrossRefGoogle Scholar
- Chandler, L. (1975). Eusociality in Ceratina calcarata Robertson (Hymenoptera: Anthophoridae). Proc. Indiana Acad. Sci. 84, 283–284.Google Scholar
- Dolzer, J., Krannich, S., Fischer, K. and Stengl, M. (2001). Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J. Exp. Biol. 204, 2781–94.Google Scholar
- Korczynska, J., Szczuka, A., Kieruzel, M., Majczynski, H., Khvorostova, N. and Godzinska, E. J. (2005). Effects of the Biogenic Amines, Dopamine, Tyramine, and Octopamine on the Behavior of Carpenter Ant Workers [Camponotus herculeanus (Hymenoptera: Formicidae)] During Nestmate Reunion Tests Carried Out After A Period of Social Isolation. Sociobiology 45, 409–447.Google Scholar
- Linn, C. E. (1997). Neuroendocrine factors in the photoperiodic control of male moth responsiveness to sex pheromone. In Insect Pheromone Research, pp. 194–209. Springer, Boston, MA.Google Scholar
- Michener, C. D. (1985). From solitary to eusocial: need there be a series of intervening species? Exp. Behav. Ecol. Sociobiol. 31, 293–305.Google Scholar
- Rehan, S. M. and Richards, M. H. (2010a). The influence of maternal quality on brood sex allocation in the small carpenter bee, Ceratina calcarata. Ethology 116, 876–887.Google Scholar
- Sakagami, S. and Maeta, Y. (1995). Task allocation in artificially induced colonies of a basically solitary bee Ceratina (Ceratsinidia) okinawana, with a comparison of sociality between Ceratina and Xylocopa (Hymenoptera, Anthophoridae, Xylocopinae). Japanese J. Ecol. 63, 115–150.Google Scholar
- Wilson, E. (1971). The Insect Societies. Cambridge, Massachusettes: Belknap/Harvard University Press.Google Scholar