Swarming Generates Rebel Workers in Honeybees

Abstract

According to kin selection theory, the colony kin structure of eusocial insects motivates workers' altruistic behaviors and therefore their sterility or restricted reproduction [1]. Indeed, theory and cross-species comparison confirm that workers engage in their own reproduction depending on relatedness among colony members [2, 3]. We show that in a honeybee colony, the workers switch from their typical altruistic role to a more selfish one if at their larval stage there are environmental cues of an upcoming decline in intracolony relatedness. This happens inevitably when a colony multiplies by swarming and replaces the mother queen with her daughter, because the mother queen's workers are faced with rearing the sister queen's offspring related to them half as much as between sisters. Workers developing from the mother queen's eggs immediately after swarming, in a temporarily queenless colony, had more ovarioles in their ovaries and less-developed hypopharyngeal glands producing brood food than control workers reared in queenright conditions. These "rebel" workers were more engaged in laying their own male-determined eggs than in rearing offspring, whether or not the sister queen was present in the colony. The finding of this previously unknown rebel strategy confirms that kin selection shapes both cooperation and conflict in honeybee societies.

When does cheating pay? Worker reproductive parasitism in honeybees

“…It has recently been shown that worker-destined larvae fed during the brief period of queenlessness following swarming have a higher number of ovarioles and are more likely to have active ovaries than those fed while a laying queen is present (Woyciechowski and Kuszewska, 2012). These reproductive individuals are known as 'rebels' as they resist the reproductive dominance of the new queen (Woyciechowski and Kuszewska, 2012), and are distinct from 'anarchists' as they only appear in the brief queenless interlude following swarming. The increase in ovary activation we observed following swarming, while not significant, may have been a manifestation of such rebel workers (Woyciechowski and Kuszewska, 2012).…”

“…These workers appear even though a new queen is present (Woyciechowski and Kuszewska, 2012). It has recently been shown that worker-destined larvae fed during the brief period of queenlessness following swarming have a higher number of ovarioles and are more likely to have active ovaries than those fed while a laying queen is present (Woyciechowski and Kuszewska, 2012). These reproductive individuals are known as 'rebels' as they resist the reproductive dominance of the new queen (Woyciechowski and Kuszewska, 2012), and are distinct from 'anarchists' as they only appear in the brief queenless interlude following swarming.…”

“…This conflict is shortlived, lasting only as long as the offspring of the old queen remain. The frequency of workers with active ovaries in colonies containing a queen varies through the year, with the highest frequency following swarming (Hoover et al, 2006, Woyciechowski and Kuszewska, 2012, Kropacova and Haslbachova, 1969. These workers appear even though a new queen is present (Woyciechowski and Kuszewska, 2012).…”

“…The frequency of workers with active ovaries in colonies containing a queen varies through the year, with the highest frequency following swarming (Hoover et al, 2006, Woyciechowski and Kuszewska, 2012, Kropacova and Haslbachova, 1969. These workers appear even though a new queen is present (Woyciechowski and Kuszewska, 2012). It has recently been shown that worker-destined larvae fed during the brief period of queenlessness following swarming have a higher number of ovarioles and are more likely to have active ovaries than those fed while a laying queen is present (Woyciechowski and Kuszewska, 2012).…”

“…Any drones laid during the period of queen production will have a greater opportunity to mate than at other times of year. It was recently shown that even in arrhenotokous A. mellifera, the degree of worker ovary activation is higher during periods of reproductive swarming (Woyciechowski and Kuszewska, 2012). In this paper we determine the maternal origin of samples of male brood collected from seven arrhenotokous A. mellifera colonies before, during and after reproductive swarming events in order to determine how whether any of these reproductive workers are successful in their attempts to reproduce.…”