Abstract

Colonies of social Hymenoptera with multiple mated queens comprise of numerous super-sister subfamilies with high within but low between subfamily relatedness. Because fitness gain in workers is indirect and relatedness dependent, inclusive fitness theory predicts that nepotism might be adaptive, particularly with respect to queen rearing and selection of new queens. However, nepotistic queen rearing could not been detected in various eusocial insect species and instead workers preferentially rear queens from rare subfamilies after queen loss. Here, we test, whether this bias can also be observed in queen rearing in preparation for reproductive swarming in the honeybee, Apis mellifera. Colonies reared swarm and subsequently emergency queens. Genotyping of all produced queens as well as worker brood revealed a significant deviation from the expected worker subfamily distribution for emergency queens but not for swarm queens. The preference of rare subfamilies may result from worker control over queen rearing in emergency queen rearing. Based on our results it appears that workers choose a few out of a vast number of worker-destined larvae to select emergency queens at extreme selection intensity. This sets the stage for competition among larvae to compete for queen caste fate, presumably by differentially attracting nurse workers to raise them as queens. During swarm queen production, workers cannot select larvae, because the queen lays eggs into predestined cells, resulting in subfamily distributions among the queens more similar to a random subfamily sample as determined in the worker brood.

Significance statement

Honeybee queens mate with multiple males resulting in several coexisting subfamilies within a colony favoring nepotism by workers rearing a super-sister as a new queen. Workers feeding queen-destined larvae a special diet and thus, larvae seem to have no influence over their caste fate. Queen rearing happens under different circumstances, conditions for nursing workers to bias queen broods and for larvae to bias their caste fate might differ. We tested for subfamily bias in queen broods reared in preparation for reproductive swarming, when queens provision specific cells with eggs to be reared as queens. Within the same colonies, after dequeening, nursing workers choose from available young larvae individuals to be reared as emergency queens. We detected a subfamily bias under emergency queens, but instead of nepotism, we found evidence for larvae to selfishly bias their own caste fate.