The role of the queen mandibular gland pheromone in honeybees (Apis mellifera): honest signal or suppressive agent?

Abstract

Queen pheromones interfere with worker reproduction in social insects. However, there is still an unresolved question as to whether this pheromone acts as an "honest" signal for workers, giving a reliable indication of the queen's reproductive value, or as a suppressive agent, inhibiting worker reproduction independent of the queen's reproductive capacity. In honeybees (Apis mellifera), the queen's mandibular gland secretion, a mix of fatty acids and some aromatic compounds, is crucial for regulating the reproductive division of labor in the colony inhibiting ovary development in workers. We quantified the mandibular gland secretions of virgin, drone-laying, and naturally mated queens using gas chromatography to test whether the queens' mating, ovary activation, or the reproductive value for workers correlated with the composition of the secretion. Although the absolute amounts of the "queen substance" 9-oxo-2(E)-decenoic acid (9-ODA) were similar among the three groups, the proportions of 9-ODA decreased with increasing reproductive quality. Furthermore, the ratios of queen to worker compounds were similar in all three treatment groups, irrespective of the reproductive capacity. A multivariate analysis including all six compounds could not separate drone-laying queens from naturally mated ones, both with active ovaries but only the latter ensuring colony survival. We suggest that the mandibular gland pheromones are unlikely to function as reliable indicators of queen reproductive value and rather operate as an agent to suppress worker reproduction. This does not exclude the possibility that other "honest" pheromone signals exist in the honeybee colony, but these would have to arise from other semiochemicals, which could be produced by both the queen and the brood.

Honest and dishonest communication in social Hymenoptera

“…dishonest, queen control. For example, the relative proportion of 9-ODA in the mandibular gland secretion was lower in highly fecund, mated honeybee queens than in both sterile and egg-laying virgin queens, and a multivariate analysis of all compounds did not separate fertile unmated and mated queens (Strauss et al, 2008). Likewise, the proportion of 3,11-dimethylheptacosane increased with the fecundity of both mated queens and unmated workers of P. inversa (d'Ettorre et al, 2004), and 9-hentriacontene also increased when unmated workers of D. quadriceps achieved social and reproductive dominance .…”

When does cheating pay? Worker reproductive parasitism in honeybees

“…Restricting the queen to one half of the hive limits the amount of comb available for her to lay eggs in, resulting in reduced amounts of brood in our excluder colonies. In A. mellifera there is a clear relationship between ovary activation and the amount of brood present; workers will activate their ovaries when the amount of brood present decreases (Mohammedi et al, 1996, Mohammedi et al, 1998, Oldroyd et al, 2001b, Pettis et al, 1997, Strauss et al, 2008. In addition, studies of A. mellifera have shown that a decrease in the amount of young brood present in colonies induces queen supersedure (Pettis et al, 1997).…”

“…Worker ovarian development is rare or absent in the presence of QMP (Hoover et al, 2003, Butler andFairey, 1963); however, the precise effect of QMP is taxonomically variable (Hoover et al, 2003, Wossler andCrewe, 1999). While workers interpret the presence of QMP as a signal of the queen's presence, they assess the fertility of the queen via signals emanating from the brood (Mohammedi et al, 1996, Mohammedi et al, 1998, Oldroyd et al, 2001b, Strauss et al, 2008. If the queen stops producing eggs, either because she is ailing or no longer present, the strength of the brood signal will decrease, eventually resulting in queen-supersedure (Pettis et al, 1997).…”

“…Workers are known to respond to this signal; they are more likely to have active ovaries in the presence of an unmated queen than when they are reared with a mated queen (Peso et al, 2013). Workers further gauge the fertility of their queen via pheromones emitted by the brood (Mohammedi et al, 1996, Mohammedi et al, 1998, Oldroyd et al, 2001b, Strauss et al, 2008, Pettis et al, 1997.…”

Reproductive traits and mandibular gland pheromone of anarchistic honey bee workers Apis mellifera occurring in China

“…QMP is dominated by the compound of 9-ODA, the so-called queen substance, which is essential for the inhibition of ovary activation and egg-laying behavior in workers (Hoover et al 2003;Dietemann et al 2007;Strauss et al 2008). Anarchistic workers are less inhibited by the queen pheromones than wild-type workers, and it has been suggested that this is due to a reduced sensitivity to queen-and larvae-produced signals Hoover et al 2005b).…”