Background

The developmental fates of offspring have the potential to be influenced by the identity of their care-givers and by the nature of the care that they receive. In animals that exhibit both parental and alloparental care, such as the annually eusocial insects, the influence of care-giver identity can be directly assessed to yield mechanistic and evolutionary insights into the origins and elaboration of brood care. Here, we performed a comparative investigation of maternal and worker brood care in bumble bees, a pollinator group where mothers (queens) rear the first offspring in the nest, and then daughters (workers) assume this role upon their emergence. Specifically, we compared the effects of queen and worker brood care on offspring development and also offspring performance, for a set of traits related to sensory biology, learning, and stress resistance.

Results

We found that queen-reared workers were smaller-bodied than worker-reared offspring, suggesting that bumble bee queens influence body size determination in their offspring. We also found that queen-reared workers were more resistant to starvation, which might be beneficial for early nesting success. These maternal influences could not be explained by feeding rate, given that we detected a similar offspring feeding frequency in both queens and workers.

Conclusion

Bumble bee queens have a unique influence on the development of the first offspring in the nest, which they rear, relative to worker-reared workers. We propose that bumble bee brood care has been shaped by a suite of evolutionary and ecological factors, which might include a maternal influence on traits that promote survival of incipient colonies.

The evolution of insect sociality has repeatedly involved changes in developmental events and their timing. Here, we propose the hypothesis that loss of a canonical regulator of moulting and metamorphosis, prothoracicotropic hormone (PTTH), and its receptor, Torso, is associated with the evolution of sociality in bees. Specifically, we posit that the increasing importance of social influences on early developmental timing in social bees has led to their decreased reliance on PTTH, which connects developmental timing with abiotic cues in solitary insects. At present, the evidence to support this hypothesis includes the absence of genes encoding PTTH and Torso from all fully-sequenced social bee genomes and its presence in all available genomes of solitary bees. Based on the bee phylogeny, the most parsimonious reconstruction of evolutionary events is that this hormone and its receptor have been lost multiple times, across independently social bee lineages. These gene losses shed light on possible molecular and cellular mechanisms that are associated with the evolution of social behavior in bees. We outline the available evidence for our hypothesis, and then contextualize it in light of what is known about developmental cues in social and solitary bees, and the multiple precedences of major developmental changes in social insects.