The alkenes Z9-C₂₉ and Z9-C₃₁ function as quorum-sensing pheromones stimulating worker reproduction in the bumble bee...

Division of labor in reproduction in eusocial insects is governed by delicate and context- dependent mechanisms, yet the regulatory processes remain largely unclear. Here, we investigate social cues involved in the establishment of reproductive dominance in bumble bee (Bombus terrestris) workers. We reveal the roles of two alkenes, (Z)-9-nonacosene (Z9- C₂₉) and (Z)-9-hentriacontene (Z9- C₃₁) in the activation of ovarian development. These alkenes are found throughout the queenright bumble bee colony, including wax, workers, drones, and gynes, and their levels are positively correlated with colony size. They act as quorum-sensing pheromones that facilitate ovary maturation in a threshold-dependent manner under queenright conditions. A synergistic interaction between the perception of these two alkenes and the occurrence of dominance contests is essential for the ovary development of worker bumble bees, independent of temporal sequence. Artificial addition of these two alkenes into colonies confirms their stimulatory effects on the ovarian developmental potential of worker bees, even in the presence of a queen. Our findings highlight a quorum-sensing-like mechanism that primes the initiation of worker ovary development, providing insights into the complex regulation of context-dependent reproductive plasticity in social insects.