Queen control of a key life-history event in a eusocial insect

Holland, Jacob G.; Guidat, Florian S.; Bourke, Andrew F. G.

doi:10.1098/rsbl.2013.0056

Cited by 19 publications

(19 citation statements)

References 16 publications

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“…A recent study in bumblebees demonstrated that queens have considerable control over their reproduction, and therefore they appear to have retained some plasticity resembling that which is seen in solitary insects, and is also seen in foundresses [41]. Caste differentiation is also more profound in bumblebees compared with Polistes.…”

Section: Discussionmentioning

confidence: 94%

Molecular heterochrony and the evolution of sociality in bumblebees ( Bombus terrestris )

et al. 2014

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Sibling care is a hallmark of social insects, but its evolution remains challenging to explain at the molecular level. The hypothesis that sibling care evolved from ancestral maternal care in primitively eusocial insects has been elaborated to involve heterochronic changes in gene expression. This elaboration leads to the prediction that workers in these species will show patterns of gene expression more similar to foundress queens, who express maternal care behaviour, than to established queens engaged solely in reproductive behaviour. We tested this idea in bumblebees (Bombus terrestris) using a microarray platform with approximately 4500 genes. Unlike the wasp Polistes metricus, in which support for the above prediction has been obtained, we found that patterns of brain gene expression in foundress and queen bumblebees were more similar to each other than to workers. Comparisons of differentially expressed genes derived from this study and gene lists from microarray studies in Polistes and the honeybee Apis mellifera yielded a shared set of genes involved in the regulation of related social behaviours across independent eusocial lineages. Together, these results suggest that multiple independent evolutions of eusociality in the insects might have involved different evolutionary routes, but nevertheless involved some similarities at the molecular level.

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Section: Discussionmentioning

confidence: 94%

Molecular heterochrony and the evolution of sociality in bumblebees ( Bombus terrestris )

et al. 2014

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“…Currently, the underlying mechanism behind the timing of the switch from the ergonomic to the reproductive phase is not known (but it has been shown that Bombus terrestris queens are able to control the switching time endogenously, Holland et al. ). Nevertheless, the framework of our model can be used to also study the evolution of eusociality, when we allow for the brood to have control over their own developmental fate.…”

Section: Discussionmentioning

confidence: 99%

“…Inherently, our model assumes that individuals in the colony possess some physiological mechanism that enables them to estimate the timing of the switch from the ergonomic phase to the reproductive phase. Currently, the underlying mechanism behind the timing of the switch from the ergonomic to the reproductive phase is not known (but it has been shown that Bombus terrestris queens are able to control the switching time endogenously, Holland et al 2013). Nevertheless, the framework of our model can be used to also study the evolution of eusociality, when we allow for the brood to have control over their own developmental fate.…”

Section: Colony Growth?mentioning

confidence: 99%

Sex‐allocation conflict and sexual selection throughout the lifespan of eusocial colonies

2019

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Models of sex‐allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen‐worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex‐allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex‐allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male‐biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex‐allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex‐allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.

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“…Such an approach is important because, in eusocial systems, the colony itself exhibits life‐history characteristics such as growth, reproduction and decline (Wilson ; Starr ; Hou et al . ; Holland, Guidat & Bourke ). In turn, this means that environmental factors, such as temperature, could have effects on colonies different from those occurring in individuals.…”

Section: Introductionmentioning

confidence: 99%

“…However, to our knowledge, no study has investigated the direct effects of temperature on life-history variables in eusocial bees at both individual and colony levels. Such an approach is important because, in eusocial systems, the colony itself exhibits life-history characteristics such as growth, reproduction and decline (Wilson 1985;Starr 2006;Hou et al 2010;Holland, Guidat & Bourke 2013). In turn, this means that environmental factors, such as temperature, could have effects on colonies different from those occurring in individuals.…”

Section: Introductionmentioning

confidence: 99%

Colony and individual life‐history responses to temperature in a social insect pollinator

Holland

Bourke

2015

Functional Ecology

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Summary1. Pollinating insects are of major ecological and commercial importance, yet they may be facing ecological disruption from a changing climate. Despite this threat, few studies have investigated the life-history responses of pollinators to experimentally controlled changes in temperature, which should be especially informative for species with complex life histories such as eusocial insects. 2. This study uses the key pollinator Bombus terrestris, a eusocial bumblebee with an annual colony cycle, to determine how temperature affects life-history traits at both individual and colony levels. 3. In two laboratory experiments, we reared B. terrestris colonies at either 20 or 25°C, and measured differences in a set of life-history traits including colony longevity, queen longevity, worker longevity, production of workers, production of sexuals (queen and male production) and growth schedule, as well as effects on thermoregulatory behaviours. 4. Higher rearing temperature had a significant positive effect on colony longevity in one of the two experiments but no significant effects on queen or worker longevity. Higher rearing temperature significantly increased colony size but did not affect the timing of peak colony size. It was also associated with significantly higher queen production but had no effect on the production of workers or males or the timing of male production. Higher temperature colonies exhibited significantly more wing fanning by workers and significantly less wax canopy construction. Hence, an increase in rearing temperature of a few degrees increased colony longevity, colony size and queen production. However, individual longevity was not affected and so may have been buffered by changes in costly thermoregulatory behaviours. 5. We conclude that eusocial insects may show complex phenotypic responses to projected temperature increases under climate change, including effects on productivity and reproduction at the colony level. Such effects should be considered when predicting the impact of climate change on the provision of essential pollination services.

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Queen control of a key life-history event in a eusocial insect

Cited by 19 publications

References 16 publications

Molecular heterochrony and the evolution of sociality in bumblebees ( Bombus terrestris )

Molecular heterochrony and the evolution of sociality in bumblebees ( Bombus terrestris )

Sex‐allocation conflict and sexual selection throughout the lifespan of eusocial colonies

Colony and individual life‐history responses to temperature in a social insect pollinator

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