Reproduction of rebel workers in honeybee (Apis mellifera) colonies

Karolina Kuszewska,Michal Woyciechowski,Agnieszka Wącławska

doi:10.1007/s13592-017-0537-z

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.

Highlights

The honeybee, the biology of which is well understood, attracts widespread interest as a honey producer and the main pollinator of crops and as a model organism for testing general biological problems, including the evolution of eusociality, focussing on the altruism of workers caring for siblings (Amdam et al 2006; Kucharski et al 2008; Ratnieks and Helanterä 2009; Graham et al 2011)
Fifteen-day-old workers reared as rebels had significantly more ovarioles than did workers of the same age reared normally. These rebel workers, which remained throughout their adult life in queenright subunits, had more activated ovaries compared with normal workers, regardless of whether these normal workers remained throughout their adult life in their subunits with the queen or remained in the orphaned subunits (GLZ; colonies 1–4; Wald’s χ 2 = 24.12; P < 0.001; colonies 1–4; Wald’s χ 2 = 26.01; P < 0.001; Figure 2b)
The results showed no differences in the size of the mandibular gland between 15-day-old rebel and normal workers, whereas the size of the hypopharyngeal gland depended on the presence of the queen during the adult life of the experimental workers

Summary

Introduction

The honeybee, the biology of which is well understood, attracts widespread interest as a honey producer and the main pollinator of crops and as a model organism for testing general biological problems, including the evolution of eusociality, focussing on the altruism of workers caring for siblings (Amdam et al 2006; Kucharski et al 2008; Ratnieks and Helanterä 2009; Graham et al 2011). The shift in resource reallocation to reproductive tissue in developing workers suggests that rebel workers, more than normal (non-rebel) workers, are physiologically prepared to lay maledestined eggs and thereby produce sons of their own (Woyciechowski and Kuszewska 2012). Workers are known to lay eggs if a colony loses its queen and there is no opportunity to rear a new one (Velthuis 1970; Page and Robinson 1994). The readiness of rebels to reproduce in queenright colonies is unexpected because of the expectation that the presence of a queen effectively inhibits worker oogenesis (Velthuis 1970; Page and Robinson 1994; Ronai et al 2015)

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