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Title: Neurohormonal changes associated with ritualized combat and the formation of a reproductive hierarchy in the ant Harpegnathos saltator

item PENICK, CLINT - North Carolina State University
item Brent, Colin
item DOLEZAL, KELLY - Arizona State University
item LIEBIG, JURGEN - Arizona State University

Submitted to: Journal of Experimental and Environmental Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/6/2014
Publication Date: 1/16/2014
Citation: Penick, C.A., Brent, C.S., Dolezal, K., Liebig, J. 2014. Neurohormonal changes associated with ritualized combat and the formation of a reproductive hierarchy in the ant Harpegnathos saltator. Journal of Experimental and Environmental Biology. 217:1496-1503.

Interpretive Summary: Some insects (ants, honey bees, termites) live in complex societies in which a few members maintain the colony population through reproduction while others forego reproduction to forage or housekeep within the nest. The members of these species are usually divided into "castes" (worker, soldier, queen) with each caste performing a different function. In some species, such as the ant, Harpengnathos saltator, select members of the worker caste can become reproductive in response to environmental and social conditions. This transformation of workers into reproductives called "gamergates" is determined through competition with other ants in the colony. Although this transformation is thought to be mediated by the brain, the specific mechanisms involved are poorly known. In controlled studies of competition, the most dominant and aggressive workers exhibited increased levels of a specific brain hormone, dopamine. In contrast, less dominant workers that were attacked by nestmates showed a decline in brain dopamine. Among workers, gamergates had the highest levels of dopamine, and dopamine levels increased with increased development of the ovaries. Workers foraging outside the nest, which are less likely to compete with nestmates to become gamergates than workers remaining in the nest, had the lowest dopamine. In addition to dopamine, levels of two other brain hormones, serotonin and tyramine, differed among the different types of workers. Overall, these results suggest that brain hormones are associated with differences in worker behavior and link dominance with the potential for reproductive development in H. saltator.

Technical Abstract: Dominance rank in animal societies is correlated with changes in both reproductive physiology and behavior. In some social insects, dominance status is used to determine a reproductive division of labor, where a few colony members reproduce while most remain functionally sterile. Changes in reproduction and behavior in this context must be coordinated through crosstalk between the brain and the reproductive system. We investigated a potential role for biogenic amines in forming this connection in the ant Harpegnathos saltator. In this species, workers engage in elaborate dominance tournaments to establish a group of reproductive workers termed gamergates. We analyzed biogenic amine content in the brains of gamergates, inside workers, and foragers under stable colony conditions and found that gamergates had the highest levels of dopamine. Dopamine levels were also positively correlated with increased ovarian activity among gamergates. Next, we experimentally induced workers to compete in a reproductive tournament to determine how dopamine may be involved in the establishment of a new hierarchy. Dopamine levels rose in aggressive workers at the start of a tournament, while workers that were policed by their nestmates (a behavior that inhibits ovarian activity) showed a rapid decline in dopamine. In addition to dopamine, levels of serotonin and tyramine differed among castes, and these changes could contribute to differences in caste-specific behavioral patterns observed among non-reproductive workers. Overall, these results provide support that biogenic amines link changes in behavior and dominance with reproductive activity in H. saltator as well as drive differences in worker task performance.