The road to sociality: brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens

doi:10.1016/j.anbehav.2019.06.004

Animal Behaviour

Volume 154, August 2019, Pages 57-65

https://doi.org/10.1016/j.anbehav.2019.06.004 Get rights and content

Highlights

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Presence of young larvae inhibited worker egg laying in B. impatiens.
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Presence of pupae stimulated worker egg laying.
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Larval effects were independent of relatedness, brood parentage or its sex.
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Larval effect was quantity dependent.
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Brood care plays an important role in the evolution of sociality.

Eusocial societies, in which egg laying is monopolized by one or a few females, have evolved multiple times during the evolution of insects but were always rooted in a simple family structure. Female reproduction in such families is often characterized by a trade-off between reproduction and brood care, yet most work on the regulation of reproduction in social insects has focused on signals and traits exhibited by adults: particularly on the behaviour and chemical signals produced by the queen and nestmate workers. Here we examined the role of brood in regulating worker reproduction in Bombus impatiens, an annual eusocial species whose reproduction is monopolized by the queen via an unknown mechanism. We found that the presence of young larvae reduced workers' egg laying, whereas the presence of pupae stimulated egg laying. The effect of young larvae was quantity dependent, with nearly complete suppression of egg laying in cages containing a pair of workers and more than 10 young larvae, and replicable regardless of worker age, relatedness to brood or brood parentage/sex. The findings that any larvae can regulate worker reproduction in this simple, yet eusocial, species highlight the role of brood in the evolution of advanced eusocial insects as a mechanism for regulating worker sterility. These findings also provide the first holistic explanation for the regulation of worker reproduction in B. impatiens, suggesting that the queen inhibits worker reproduction through her brood.

Section snippets

General Bumblebee Rearing

Colonies of B. impatiens were obtained from BioBest (Canada) and were maintained in laboratory nestboxes under constant darkness, at a temperature of 28–30 °C and 60% relative humidity, and supplied ad libitum with a sugar solution and fresh pollen (Light spring bee pollen, 911Honey). These colonies were used as a source of callows (newly emerged workers <24 h), random workers of an unknown age and brood. All workers were sampled from young, precompetition colonies containing a queen. At this

Results

The type of brood significantly affected the number of eggs laid by workers (GLM: χ²₅ = 66.7, P < 0.001; Fig. 1a). Pairwise contrasts between all treatments showed that workers in the EL (eggs that developed into larvae) and LL (young larvae that remained larvae) groups laid significantly fewer eggs compared with all other treatments (P < 0.001). Workers in the PP (pupae that remained pupae) groups laid significantly more eggs compared with EL, LL and wax treatments (P < 0.001), and workers in the LP

Acknowledgments

We thank members of the Amsalem Lab for helpful discussions and critical reading of earlier drafts of the manuscript and two anonymous referees for critical evaluation of the manuscript.

References (65)

E. Amsalem et al.
The physiological and genomic bases of bumble bee social behaviour
Advances in Insect Physiology
(2015)
J.B. Free et al.
Brood recognition by honeybee (Apis mellifera) workers
Animal Behaviour
(1983)
W.D. Hamilton
The genetical evolution of social behaviour I
Journal of Theoretical Biology
(1964)
K.R. Helms et al.
Sex ratio determination by queens and workers in the ant Pheidole desertorum
Animal Behaviour
(2000)
R. Kilner et al.
Begging the question: Are offspring solicitation behaviours signals of need?
Trends in Ecology & Evolution
(1997)
D.J. Kronauer et al.
Back to the roots: The importance of using simple insect societies to understand the molecular basis of complex social life
Current Opinion in Insect Science
(2018)
S.D. Leonhardt et al.
Ecology and evolution of communication in social insects
Cell
(2016)
F. Mas et al.
Maternal care and offspring begging in social insects: Chemical signalling, hormonal regulation and evolution
Animal Behaviour
(2008)
E.D. Sibbald et al.
Social interactions and their connection to aggression and ovarian development in orphaned worker bumblebees (Bombus impatiens)
Behavioural Processes
(2014)
J. Stokl et al.
Evolutionary origin of insect pheromones
Current Opinion in Insect Science
(2017)

I. Villalta et al.

Regulation of worker egg laying by larvae in a fission-performing ant

Animal Behaviour

(2015)

C. Alaux et al.

Queen influence on worker reproduction in bumblebees (Bombus terrestris) colonies

Insectes Sociaux

(2004)

C. Alaux et al.

Regulation of worker reproduction in bumblebees (Bombus terrestris): Workers eavesdrop on a queen signal

Behavioral Ecology and Sociobiology

(2006)

E. Amsalem et al.

The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers

Behavioral Ecology and Sociobiology

(2010)

E. Amsalem et al.

The effect of group size on the interplay between dominance and reproduction in Bombus terrestris

PLoS One

(2011)

E. Amsalem et al.

A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens)

Proceedings of the Royal Society B: Biological Sciences

(2015)

E. Amsalem et al.

Do bumble bee, Bombus impatiens, queens signal their reproductive and mating status to their workers?

Journal of Chemical Ecology

(2017)

E. Amsalem et al.

Reproductive competition in the bumble-bee Bombus terrestris: Do workers advertise sterility?

Proceedings of the Royal Society B: Biological Sciences

(2009)

W.S. Bigley et al.

Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta

Annals of the Entomological Society of America

(1975)

G. Bloch

Regulation of queen–worker conflict in bumble-bee (Bombus terrestris) colonies

Proceedings of the Royal Society B: Biological Sciences

(1999)

G. Bloch et al.

Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies

Journal of Chemical Ecology

(1999)

G. Bloch et al.

Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies

Behavioral Ecology and Sociobiology

(1999)

S.P.A. den Boer et al.

A larval hunger signal in the bumblebee Bombus terrestris

Insectes Sociaux

(2006)

J. Cnaani et al.

Colony development, larval development and worker reproduction in Bombus impatiens Cresson

Insectes Sociaux

(2002)

B.N. Danforth et al.

The impact of molecular data on our understanding of bee phylogeny and evolution

Annual Review of Entomology

(2013)

M.J. Duchateau et al.

Development and reproductive strategies in Bombus terrestris colonies

Behaviour

(1988)

J.D. Ebie et al.

Larval regulation of worker reproduction in the polydomous ant Novomessor cockerelli

Naturwissenschaften

(2015)

A. Endler et al.

Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect

Proceedings of the National Academy of Sciences of the United States of America

(2004)

K.C. Engel et al.

A hormone-related female anti-aphrodisiac signals temporary infertility and causes sexual abstinence to synchronize parental care

Nature Communications

(2016)

B.M. Glancey et al.

Pheromone may induce brood tending in the fire ant, Solenopsis saevissima

Nature

(1970)

J. Heinze et al.

Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa

Journal of Insect Behavior

(1996)

C.G.J. van Honk et al.

The mandibular glands of Bombus terrestris queens as a source of queen pheromone

Entomologia Experimentalis et Applicata

(1980)

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The road to sociality: brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens

Highlights

Section snippets

General Bumblebee Rearing

Results

Acknowledgments

Advances in Insect Physiology

Animal Behaviour

Journal of Theoretical Biology

Animal Behaviour

Trends in Ecology & Evolution

Current Opinion in Insect Science

Cell

Animal Behaviour

Behavioural Processes

Current Opinion in Insect Science

Animal Behaviour

Queen influence on worker reproduction in bumblebees (Bombus terrestris) colonies

Insectes Sociaux

Regulation of worker reproduction in bumblebees (Bombus terrestris): Workers eavesdrop on a queen signal

Behavioral Ecology and Sociobiology

The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers

Behavioral Ecology and Sociobiology

The effect of group size on the interplay between dominance and reproduction in Bombus terrestris

PLoS One

A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens)

Proceedings of the Royal Society B: Biological Sciences

Do bumble bee, Bombus impatiens, queens signal their reproductive and mating status to their workers?

Journal of Chemical Ecology

Reproductive competition in the bumble-bee Bombus terrestris: Do workers advertise sterility?

Proceedings of the Royal Society B: Biological Sciences

Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta

Annals of the Entomological Society of America

Regulation of queen–worker conflict in bumble-bee (Bombus terrestris) colonies

Proceedings of the Royal Society B: Biological Sciences

Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies

Journal of Chemical Ecology

Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies

Behavioral Ecology and Sociobiology

A larval hunger signal in the bumblebee Bombus terrestris

Insectes Sociaux

Colony development, larval development and worker reproduction in Bombus impatiens Cresson

Insectes Sociaux

The impact of molecular data on our understanding of bee phylogeny and evolution

Annual Review of Entomology

Development and reproductive strategies in Bombus terrestris colonies

Behaviour

Larval regulation of worker reproduction in the polydomous ant Novomessor cockerelli

Naturwissenschaften

Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect

Proceedings of the National Academy of Sciences of the United States of America

A hormone-related female anti-aphrodisiac signals temporary infertility and causes sexual abstinence to synchronize parental care

Nature Communications

Pheromone may induce brood tending in the fire ant, Solenopsis saevissima

Nature

Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa

Journal of Insect Behavior

The mandibular glands of Bombus terrestris queens as a source of queen pheromone

Entomologia Experimentalis et Applicata