Honeybees possess a structurally diverse and functionally redundant set of queen pheromones

Abstract

Queen pheromones, which signal the presence of a fertile queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the queen's mandibular glands have been argued to act as the primary sterility-inducing pheromones. This contrasts with evidence from other groups of social insects, where specific queen-characteristic hydrocarbons present on the cuticle act as conserved queen signals. This led us to hypothesize that honeybee queens might also employ cuticular pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee queen signal mix are discussed.

Drosophila melanogaster and worker honeybees (Apis mellifera) do not require olfaction to be susceptible to honeybee queen mandibular pheromone

“…In insects, reproductive dominance is established by behavioural aggression and/or chemical cues (Le Conte and Hefetz, 2008;Padilla et al, 2016). Chemical cues are often in the form of queen pheromones (Matsuura et al, 2010;Van Oystaeyen et al, 2014;Princen et al, 2019;Vargo and Laurel, 1994;Winston and Slessor, 1992). Perhaps the most well-studied queen pheromone is Queen Mandibular Pheromone (QMP), produced by queen honeybees (Apis mellifera) (Keeling et al, 2003;Pankiw et al, 1996;Slessor et al, 1988).…”

Identification of a queen pheromone mediating the rearing of adult sexuals in the pharaoh ant Monomorium pharaonis

“…For example, in the well-studied honeybee Apis mellifera, the queen mandibular pheromone blend induces worker sterility, promotes queen retinue behaviour and acts as a sex attractant pheromone [34][35][36][37][38]. Likewise, in both honeybees and the common wasp Vespula vulgaris queen pheromones that stop workers from reproducing are also used as egg-marking pheromones [39][40][41]. Convergent evolution has also caused neocembrene to be used both as a sex pheromone and a trail-following pheromone in several termite species [42].…”

Neotropical Social Wasps

“…In this species, a honeybee-specific blend of pheromones derived from the queen's mandibular gland (QMP), containing the keto acid 9-oxo-decenoic acid as major compound, was shown to inhibit worker reproduction (Butler 1959;Hoover et al 2003). Recent work, however, has shown that specific cuticular wax compounds act as more conserved queen pheromones across several groups of Hymenoptera, including wasps, ants, bumblebees, and the honeybee (Van Oystaeyen et al 2014, reviewed in Oi et al 2015bPrincen et al 2019a). The fact that structurally related and sometimes even identical hydrocarbon compounds were found to suppress worker reproduction across these different independently evolved lineages of social insects implies very strong evolutionary conservation and suggested that these signals likely evolved from preexisting fertility-linked compounds that were already present in the common solitary ancestors of all extant social Hymenoptera (Van Oystaeyen et al 2014;Oi et al 2015b).…”