Cross-activity of honeybee queen mandibular pheromone in bumblebees provides evidence for sensory exploitation

Abstract

The evolutionary origin of queen pheromones (QPs), which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect QPs—such as cuticular hydrocarbons—were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on preexisting gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee QP pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.

Pheromonal Regulation of the Reproductive Division of Labor in Social Insects

“…On the other hand, the QMPs unexpectedly showed reduced ovary size, number of eggs and the number of viable offspring in phylogenetically distantly related fruit fly Drosophila melanogaster, suggesting the exploitation of conserved physiological pathways (Camiletti et al, 2013;Galang et al, 2019). This finding was further verified by a recent study demonstrating a remarkable cross activity of honeybee QMP in bumblebees, in which the egg laying of workers and queens are inhibited by non-native QMP blend (Princen et al, 2019). Another hypothesis under the sensory exploitation scenario is that QPs evolve from oviposition deterring pheromones.…”

“…This sensory exploitation could be evolutionarily stable in the long run, by leading to either a queen-worker arm race, to workers evolving counter-adaptations, or to limited personal cost of workers' sterility (Kocher and Grozinger, 2011;Peso et al, 2015). From a proximate perspective, the evolution of manipulative QPs requires the queens to be immune to the pheromones themselves, considering the inhibitory effect of honeybee QMP on bumblebee queens (Princen et al, 2019).…”

Honeybee Queen mandibular pheromone induces starvation in Drosophila melanogaster, implying a role for nutrition signalling in the evolution of eusociality

“…That QMP phenocopies or induces a starvation response in D. melanogaster implies that QMP interferes with nutrition signalling, or perception, in this species. That this effect is not limited to D. melanogaster (Camiletti et al, 2013;Lovegrove et al, 2019;Sannasi, 1969), but also occurs in a wide range of arthropods (Carlisle and Butler, 1956;Hrdy et al, 1960;Nayar, 1963;Princen et al, 2020;Sannasi and George, 1972) implies that whatever is being affected by QMP is conserved and present broadly in arthropods. It therefore seems likely that QMP is disrupting highly conserved nutrition perception or signalling pathways in these species.…”

“…QMP not only has the ability to repress reproduction in worker honeybees, but in non-target arthropods as well. It has been shown to repress reproduction in Drosophila melanogaster (Camiletti et al, 2016;Lovegrove et al, 2019;Sannasi, 1969) , a house fly (Musca domestica) (Nayar, 1963), bumble bee (Bombus terrestris) (Princen et al, 2020), an ant (Formica fusca) (Carlisle and Butler, 1956), termite (Kalotermes flavicollis) (Hrdy et al, 1960) and a prawn (Leander serratus) (Carlisle and Butler, 1956); species that shared a last common ancestor more than 530 million years ago (dos Reis et al, 2015). This ability to repress reproduction in a broad range of species is a novel feature, unique to QMP, and not a conserved function of hymenopteran queen pheromones (Lovegrove et al, 2019).…”

Chemical Variation among Castes, Female Life Stages and Populations of the Facultative Eusocial Sweat Bee Halictus rubicundus (Hymenoptera: Halictidae)

“…Different letters indicate significant differences. Different letters indicate significant differences between the groups lineages (Oi et al 2015(Oi et al , 2016Princen et al 2020;Van Oystaeyen et al 2014). This suggests that population 'dialects' may not represent caste-specific chemical signals such as queen signals, but may rather influence signals mediating kin or nestmate recognition in social insects.…”