Egg viability and worker policing in honey bees

Abstract

In many species of social Hymenoptera, unmated workers can lay eggs that will produce males by parthenogenesis. Nevertheless, in queenright honey bee colonies (Apis mellifera), worker reproduction is low. One possible mechanism for this difference is worker policing, the removal of worker-laid eggs by other workers. This behavior can evolve in species in which queens are multiply mated, where workers are more closely related to the sons of their mother than those of their sisters. Another possible mechanism of the low level of worker reproduction is worker-laid eggs being less viable than queen-laid eggs. We show that this difference in quality is the case for honey bees. W orker reproduction is low in honey bee (Apis mellifera) colonies with a queen (1, 2), because a suite of pheromones derived from the queen and the brood inhibits ovarian development in workers (3). Moreover, workers with developed ovaries are attacked by other workers (4). Nevertheless, a considerable proportion (Ϸ4%) of workers can have functional ovaries (5) and can lay a substantial number (7%) of male eggs (6). Therefore, a crucial factor restricting successful worker reproduction in honey bees seems to be the removal of workerlaid eggs by other workers (worker policing) (7). Worker policing has been the focus of many theoretical and empirical studies in a wide range of species of social Hymenoptera (7-12). This behavior is considered adaptive in species in which queens mate multiply, causing workers to be on average more closely related to the son's of the queen than with sons of other workers (8,9).It has been postulated that queen honey bees mark their eggs with a queen-specific pheromonal label, providing the proximate cue for worker discrimination between queen-laid and workerlaid eggs (13). However, neither the source nor chemical nature of this postulated label has yet been identified (14-16). In contrast, the removal of diseased and dead brood by workers (hygienic behavior) is more fully understood (17). Workers remove dead brood within a few hours of death, an important factor in resisting disease (18). If there is a high mortality rate in worker-laid eggs, this alone would plausibly explain the removal of worker-laid eggs.The question of a difference in the viability of queen-laid and worker-laid male eggs has been addressed in an in vitro incubation experiment (7) and yielded no significant differences between the two types of eggs. However, the egg viability was extremely, and probably abnormally, low for both types of eggs because of the in vitro experimental conditions in this study (7). This low viability may have masked normal differences in egg viability. We therefore examined the relative viability of queenlaid and worker-laid male eggs in vivo in natural brood nests of honey bee colonies. We also compared our viability data with egg removal data for queen-laid and worker-laid male eggs in the same colonies. The data show a striking correspondence between egg viability and egg removal, suggesting that hygienic behavior m...

Altruism in insect societies and beyond: voluntary or enforced?

“…In addition, in some species, policing workers gain direct reproductive benefits because they lay eggs themselves [38,71,72]. Finally, Pirk et al suggested that worker policing in the honeybee is aimed at removing unviable worker-laid eggs [73]. This idea, however, has since been disproven since dead queen-laid eggs are not policed in the honeybee [74], contrary to what is expected if egg policing is merely a form of hygienic behaviour aimed at removing dead individuals.…”

Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory

“…At present, it is unknown whether queens ever police worker-laid eggs. Velthuis et al (2002) and Pirk et al (2004) suggested that worker-laid eggs have lower viability than queenlaid ones, and that workers merely police dead eggs. This idea, however, has since been disproven (Beekman and Oldroyd 2005).…”

“…Since the queen did not visit the comb with introduced eggs during the larger part of the trials, queen policing was probably absent (Foster and Ratnieks 2001a). It has also been shown that worker-laid eggs have a similar viability as queen-laid ones (Helanterä et al 2006), thereby eliminating the possibility that workers might police for hygienic reasons (Pirk et al 2004). ANTS: A. echinatior.…”

“…This is unlikely for most species, except for those with extremely small colonies in which the cost exacted by a single nonworking reproductive worker might indeed be as high as 25% (e.g., in the Sphecid wasp Microstigmus comes, which can have colonies of only three or four females [Ross and Matthews 1989]). In another efficiency-based argument, Pirk et al (2004) have argued that worker-laid eggs in the honeybee are inviable and that worker policing can be explained simply as the removal of dead (worker-laid) eggs. This hypothesis, however, is weak for several reasons (Beekman and Oldroyd 2005).…”

“…This has led to doubts concerning the importance of relatedness in selecting for worker policing (Foster et al 2002;Hartmann et al 2003;Pirk et al 2003Pirk et al , 2004Endler et al 2004;Gadagkar 2004;Wilson 2005). This doubt was reinforced by , who used a comparative analysis of 50 species of ants, bees, and wasps to show that the proportion of males that are workers' sons is not influenced by relatedness.…”