Cooperative animal societies are extremely successful but their evolution still is not well understood. A framework for understanding social evolution is offered by the emerging reproductive ground-plan hypothesis, which suggests that the reproductive regulatory pathways of non-social ancestors were co-opted during evolution to control social phenotypes. According to this hypothesis, reproductive gene-networks should govern the complex specialization of different colony members that guarantee the functioning of the societies. The hypothesis links regulatory mechanisms of physiology and behavior to a plausible evolutionary scenario, leading to a unified theory of social evolution. Recent mathematical simulation models and behavioral studies suggest that the fundamental characteristics of social insects (reproductive division of labor and co-operative specialization of worker behavior) indeed are derived from an ancestral reproductive cycle. This project will take advantage of these encouraging results and conduct the first direct test of the reproductive ground-plan hypothesis at the genetic level, using the honey bee as experimental model. Worker honey bees show a set of correlated behavioral, life-history, and physiological traits; including sensory sensitivity, behavioral maturation, reproductive tuning, foraging preference and length of life. Such complex trait-associations are predicted by the reproductive ground-plan hypothesis. Specific honey bee genomic regions have been identified that affect the rate of behavioral maturation and foraging preference for nectar or pollen. Two breeding lines (selected for high and low pollen-hoarding behavior) and two races (Africanized and European) of honey bees will be used to investigate the predicted link between the genetic architectures of reproduction and of social behavior. Reproduction will be measured as ovary size and ovary activity. For both reproductive traits, the first goal is to characterize the inheritance pattern through a series of experimental crosses. Next, it will be investigated whether the genetic control of these traits is tied to the previously identified genomic regions that influence social behavior, and which other regions are influential. Finally, all potential genes in the influential genomic regions will be identified from the honey bee genome sequence to produce a prioritized candidate gene list based on positional and functional criteria. The activity patterns of the top candidate genes will be studied, and their function will be determined by means of specific gene expression manipulations. Genetic and functional gene overlap between reproductive traits and social behavior will support the reproductive ground-plan hypothesis of social evolution, no overlap will refute it. Thus, this project will critically test a major unifying explanation of sociality, which is an endeavor of broad scientific implication and interest. A significant portion of this research will involve interactive student research, particularly at the undergraduate level. Students will get first-class research experiences in cutting-edge molecular techniques. Broader impacts also extend to the departmental, institutional, and regional level.
