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An organizing feature of bumble bee life history: worker emergence promotes queen reproduction and survival in young nests.

ABSTRACT: Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests.

SUBMITTER: Sarro E

PROVIDER: S-EPMC8242224 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundEfficient division of reproductive labor is a crucial characteristic of social insects and underlies their ecological and evolutionary success. Despite of the harmonious appearance of insect societies, nestmates may have different interests concerning the partitioning of reproduction among group members. This may lead to conflict about reproductive rights. As yet, few studies have investigated the allocation of reproduction among queens in multi - queen societies ("reproductive skew"). In the ant Leptothorax acervorum, reproductive skew varies considerably among populations. While reproduction is quite equally shared among nestmate queens in most populations from boreal Eurasia (low skew), colonies from populations at the edge of the species' range are characterized by "functional monogyny," i.e., high skew. The proximate mechanisms underlying high skew, in particular how workers influence which queen lays eggs, are not well understood. We investigated the behavior of queens and workers in functionally monogynous colonies of L. acervorum from two mountain ranges in central Spain.ResultsWe provide evidence for both queen and worker influence on the outcome of conflict over reproduction in colonies of L. acervorum from Spain. The patterns of queen - queen aggression and worker - queen grooming and feeding after hibernation allowed predicting, which queen later began to lay eggs. In contrast, worker aggression towards queens was not clearly associated with a queen's future reproductive success. Queen - queen and worker - queen aggression differed in quality: queens typically engaged in ritualized dominance behavior, such as antennal boxing, while workers also attacked queens by biting and prolonged pulling on their legs and antennae. In several cases, overt worker aggression led to the expulsion of queens from the nest or their death.ConclusionWe conclude that queens of L. acervorum from Spain establish rank orders by ritualized dominance interactions, such as antennal boxing. Workers may reinforce these hierarchies by preferentially feeding and grooming high ranking queens and attacking lower ranking queens. Aggressive worker policing may thus stabilize functional monogyny. Optimal skew models predict that high skew in ants is associated with high dispersal costs. In central Spain, L. acervorum is restricted to small patches at higher elevations, which presumably makes dispersal and colony founding difficult. Because of the ecological requirements of L. acervorum and the predicted large impact of global change on central Spain, the functionally monogynous populations of this ant must be considered as threatened.

Project description:Reproductive division of labor is one of the defining traits of honey bees (Apis mellifera), with non-reproductive tasks being performed by workers while a single queen normally monopolizes reproduction. The decentralized organization of a honey bee colony is maintained in large part by a bouquet of queen-produced pheromones, the distribution of which is facilitated by contact among workers throughout the hive. Previous studies have shown that the developmental fate of honey bee queens is highly plastic, with queens raised from younger worker larvae exhibiting higher measures of reproductive potential compared to queens raised from older worker larvae. We investigated differences in the chemical composition of the mandibular glands and attractiveness to workers of "high-quality" queens (i.e., raised from first instar worker larvae; more queen-like) and "low-quality" queens (i.e., raised from third instar worker larvae; more worker-like). We characterized the chemical profiles of the mandibular glands of high-quality queens and low-quality queens using GC-MS and used the worker retinue response as a measure of the attractiveness to workers of high-quality queens vs. low-quality queens. We found that queen quality affected the chemical profiles of mandibular gland contents differently across years, showing significant differences in the production of the queen mandibular pheromone ("QMP") components HVA and 9-HDA in 2010, but no significant differences of any glandular compound in 2012. We also found that workers were significantly more attracted to high-quality queens than to low-quality queens in 2012, possibly because of increased attractiveness of their mandibular gland chemical profiles. Our results indicate that the age at which honey bee larvae enter the "queen-specific" developmental pathway influences the chemical composition of queen mandibular glands and worker behavior. However, these changes are not consistent across years, suggesting that other external factors may play important roles in modulating queen quality.

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An organizing feature of bumble bee life history: worker emergence promotes queen reproduction and survival in young nests.

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