Care-giver identity impacts offspring development and performance in an annually social bumble bee

Claudinéia P Costa,Naoki Yamanaka,Guy Bloch,Kaleigh Fisher,Blanca M Guillén,S Hollis Woodard

doi:10.1186/s12862-021-01756-2

Claudinéia P Costa, Naoki Yamanaka + Show 4 more

Open Access

https://doi.org/10.1186/s12862-021-01756-2

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Abstract

BackgroundThe 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.ResultsWe 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.ConclusionBumble 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.

Highlights

The developmental fates of offspring have the potential to be influenced by the identity of their caregivers and by the nature of the care that they receive
We explored differences in the quality or performance of adult offspring reared by either a single queen or a set of workers, for a set of traits related to sensory biology, learning, and stress resistance
We propose that our finding that queen-reared workers are more resistant to starvation might be related to the action of selection favoring worker traits that are beneficial during the early nesting period, a time when nests might be sensitive to food shortages [42] and when many wild bumble bee nests likely fail [20, 21, 45]

Summary

Introduction

The developmental fates of offspring have the potential to be influenced by the identity of their caregivers and by the nature of the care that they receive. A small subset of eusocial insect species exhibit both maternal and sibling care, albeit at different life history stages This is seen in the eusocial species where nests are founded by a solitary queen, which includes some primitively eusocial bees, including bumble bees (genus Bombus, family Apidae), and others hymenopterans, such as paper wasps (genus Polistes, family Vespidae) and the solitary founding ants. In these systems, queens care for their brood during initial stages of colony development, cease providing care around the time that workers eclose in the nest and begin to care for their siblings [14,15,16,17]. Nests are subject to other stressors, such as pesticides, and many solitarily-founded nests likely fail at the initiation stage, which precludes the production of new reproductives (new queens and males) [20, 21]

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