Reproduction of rebel workers in honeybee (Apis mellifera) colonies

Abstract

-The honeybee is one of several eusocial species in which the queen is typically the only reproductive member of the colony; worker reproduction is mostly restricted to queenless colonies. Because workers cannot mate, they lay unfertilized eggs, which develop into males. A recent study showed that in queenless colonies, which arise after swarming, worker larvae develop into rebel workers that have greater reproductive potential than do workers reared in queenright colonies, as measured by the number of ovarioles and degree of ovary activation. However, there was no evidence that rebels had an opportunity to produce male offspring. Here, we show for the first time that rebel workers not only activate their ovaries but also produce significantly more male offspring in queenright colonies than do normal workers. Moreover, our results show that the level of rebel reproduction in queenright colonies is similar to the reproduction of normal workers in queenless colonies. This finding suggests that the ultimate factor favouring the evolution of the rebel strategy is the decrease in relatedness between the old-generation workers and the new queen's offspring that occurs after queen exchange at swarming.Apis mellifera / rebel workers / worker reproduction / kin selection

Do rebel workers in the honeybee Apis mellifera avoid worker policing?

“…However, the source of chemical labels has yet to be identified (Katzav-Gozansky et al 2002;Martin et al 2002;Oldroyd et al 2002). The shift in resource reallocation to reproductive tissue during development causes rebel workers, more so than normal workers, to be physiologically prepared to lay male-destined eggs and thereby produce sons of their own (Woyciechowski and Kuszewska 2012;Kuszewska et al 2017). However, the results of our experiment show that the rebel workers do not evade worker policing by laying more acceptable eggs.…”

“…These features suggest that the rebel workers are more engaged in laying their own male-determined eggs than in rearing the queen's offspring. A recent study confirmed this suggestion, as Kuszewska et al (2017) showed that rebels lay their own eggs even in the presence of the queen. Another study showed that 15-day-old rebel workers exhibited active ovaries if they remained in a queenless or a q u e e n r i g h t c o l o n y d u r i n g a d u l t h o o d (Woyciechowski and Kuszewska 2012).…”

“…Those authors found that after swarming, during which rebel workers usually develop, the number of workers with active ovaries increases, but the number of drones in this period does not change (Holmes et al 2013). However, recent studies regarding the reproductive potential of workers show that rebel workers have more adult sons than normal workers in queenright colonies (Kuszewska et al 2017). Consequently, rebel workers not only have a higher reproductive potential than normal workers on the first day of their adult life but also produce male offspring under both queenless and queenright conditions.…”

Honeybee rebel workers preferentially respond to high concentrations of sucrose

“…All colonies were treated in the same way, and the experimental design was previously described by Woyciechowski and Kuszewska (2012) as well as in other papers (i.a. Kuszewska et al 2017Kuszewska et al , 2018bWoyciechowski et al 2017). At the beginning of the experiment, the queen was restricted to two experimental frames to produce eggs of a similar age (day 0).…”

Rebel honeybee workers have a tendency to become intraspecific reproductive parasites

“…The proximate factor that influences rebel caste development is the absence of a queen or, more precisely, the lack of a queen's mandibular gland pheromones (Woyciechowski, Kuszewska, Pitorak, & Kierat, 2017) during the larval feeding period (unsealed larvae). If they remain in a queenless or a queenright colony during their adult lifetimes, these rebel workers display active ovaries (Woyciechowski & Kuszewska, 2012) and have a higher number of male offspring than normal workers (Kuszewska, Wącławska, & Woyciechowski, 2018). The appearance of workers with mature ovaries in orphaned colonies is not surprising as workers are known to lay eggs when a colony loses its queen and there is no chance of rearing a new queen (Page & Robinson, 1994;Velthuis, 1970).…”