A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.)

Abstract

Eusocial insects live in teeming societies with thousands of their kin. In this crowded environment, workers combat disease by removing or burying their dead or diseased nestmates. For honey bees, we found that hygienic brood-removal behavior is triggered by two odorants – β-ocimene and oleic acid – which are released from brood upon freeze-killing. β-ocimene is a co-opted pheromone that normally signals larval food-begging, whereas oleic acid is a conserved necromone across arthropod taxa. Interestingly, the odorant blend can induce hygienic behavior more consistently than either odorant alone. We suggest that the volatile β-ocimene flags hygienic workers’ attention, while oleic acid is the death cue, triggering removal. Bees with high hygienicity detect and remove brood with these odorants faster than bees with low hygienicity, and both molecules are strong ligands for hygienic behavior-associated odorant binding proteins (OBP16 and OBP18). Odorants that induce low levels of hygienic behavior, however, are weak ligands for these OBPs. We are therefore beginning to paint a picture of the molecular mechanism behind this complex behavior, using odorants associated with freeze-killed brood as a model.

Dead cells release a ‘necrosignal’ that activates antibiotic survival pathways in bacterial swarms

“…A large motile population, that can continuously acquire new territory, and that has a strategy to overcome stressful environments and survive mass extinction events promoted by the event itself, will also increase its chances of propagating beneficial mutations such as antibiotic resistance. We note that a response to cell death that benefits the living is not confined to bacteria, but is widespread in nature, as seen in insects (necromones) 63,64 , fishes 65 , birds 66 , and mammals 67 , possibly even in eukaryotic tumors 68 .…”

Necrosignaling: Cell death triggers antibiotic survival pathways in bacterial swarms

“…A large motile population, that can continuously acquire new territory, and has a strategy to overcome stressful environments and survive mass extinction events promoted by the event itself, will also increase its chances of propagating beneficial mutations such as antibiotic resistance. We note that a response to cell death that benefits the living is not confined to bacteria, but is widespread in nature, as seen in insects (necromones) 48,49 , fishes 50 , birds 51 , and mammals 52 , possibly even in eukaryotic tumors 53 .…”

Managing the risks and rewards of death in eusocial insects

“…After death, they rapidly peak in quantity to recruit undertakers in a timely manner and then gradually decrease. In the honeybee Apis mellifera , a volatile brood pheromone, β-ocimene, which signals food begging, continues to emit after death and recruits workers to uncap and remove dead larvae [ 23 ]. The above-mentioned examples represent three distinct patterns of using chemicals produced prior to death for the timely detection of death: diminished vital signs, increased early death cues and co-option of pheromones, respectively.…”

“…In a pioneering study of chemical stimuli for corpse disposal, Wilson et al [ 16 ] found that oleic acid was the most effective stimulus eliciting corpse removal in two ant species, Pogonomyrmex badius and Solenopsis saevissima . Since then, ‘fatty acid death cues’ have been found in many other social species, including the archaic ant Myrmecia vindex [ 39 ], the red ant Myrmica rubra [ 20 ], the fire ant Solenopsis invicta [ 40 ], a fungus-growing termite Pseudacanthotermes spiniger [ 41 ], two subterranean termites Reticulitermes virginicus [ 42 ] and R. flavipes [ 18 ], as well as the honeybee A. mellifera [ 23 ]. Oleic acid and linoleic acid are the most common stimuli for corpse disposal in those species; the two compounds have low volatilities and require direct contact or short distance detection.…”

“…In the fire ant S. invicta , a chemosensory protein gene, Si-CSP1 , was found to be responsible for detecting oleic acid and linoleic acid and thus mediating corpse removal [ 22 ]. In the honeybee A. mellifera , both oleic acid and β-ocimene are ligands for two OBPs (OBP16 and OBP18), which are associated with hygienic behaviour (removal of diseased brood) [ 23 , 57 ]. Receptors for either conserved fatty acid death cues or species/taxon-specific death cues remain unknown in insects.…”