“Queen longevity and fecundity affect conflict with workers over resource inheritance in a social insect”

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Edward J. Almond, Timothy J. Huggins, Liam P. Crowther, Joel D. Parker, and Andrew F. G. Bourke (Feb 2019)

The DOI will be https://dx.doi.org/10.1086/701299

Bumblebee workers harass queens with simulated fecundity loss: new support for kin conflict over resource inheritance

Queen-worker conflict in bumblebee colonies

Colony of the Buff-tailed Bumblebee, Bombus terrestris, with workers, queen (lower right-hand corner), and brood cells.
(Credit: Andrew Bourke, University of East Anglia)

Bumblebee workers, highly valued as pollinators, have a distinctly less wholesome social life. Within the colony, they appear to make self-interested calculations about whether or not to keep supporting the queen. When a queen bumblebee dies, some of the workers can lay eggs and produce offspring. A team led by Andrew Bourke at the University of East Anglia and Joel Parker then at the University of Southampton and currently at the State University of New York, Plattsburgh, has shown that bumblebee workers behave in accordance with a model predicting conflict with the queen over the timing of the queen’s death.

Many animals pass on their nest, den, or territory to their offspring when they die. But such resource inheritance need not happen smoothly. According to the theory of kin-selected conflict, parents and offspring differ in the optimal timing of resource handover. The underlying reason is that, following inheritance, parents effectively gain grandoffspring, but the offspring inheriting the resource gain offspring of their own, to which they are comparatively more closely related. So, in terms of evolutionary fitness, the trade is more favorable to offspring than to parents.

The team tested a model of this situation using captive colonies of the Buff-tailed Bumblebee, Bombus terrestris. They found that, as the model assumed, the workers gain more direct fitness the longer they can reproduce after the queen’s death. Moreover, queen fecundity falls with time, which means the threshold for deposing the queen is met first for those workers laying eggs after her death. When the team simulated (by daily removal of her eggs) the queen losing all her fecundity, these workers, as predicted, increased their rate of harassment of the queen. Overall, the study provides new support for kin-selected conflict over resource inheritance being a key process in social animals.


Abstract

Resource inheritance is a major source of conflict in animal societies. However, the assumptions and predictions of models of conflict over resource inheritance have not been systematically tested within a single system. We developed an inclusive fitness model for annual eusocial Hymenoptera that predicts a zone of conflict in which future reproductive workers are selected to enforce nest inheritance before the queen is selected to cede the nest. We experimentally tested key elements of this model in the bumble bee Bombus terrestris. In colonies from which queens were sequentially removed, queen tenure was significantly negatively associated with worker male production, confirming that workers gain direct fitness by usurping the queen. In unmanipulated colonies, queen fecundity decreased significantly over the latter part of the colony cycle, confirming that workers' indirect fitness from maintaining queens declines over time. Finally, in an experiment simulating loss of queen fecundity by removal of queens' eggs, worker-to-queen aggression increased significantly and aggressive workers were significantly more likely to become egg-layers, consistent with workers monitoring queen fecundity to assess the net benefit of future reproduction. Overall, by upholding key assumptions and predictions of the model, our results provide novel empirical support for kin-selected conflict over resource inheritance.