Social immunity in honeybees—Density dependence, diet, and body mass trade‐offs

Abstract Group living is favorable to pathogen spread due to the increased risk of disease transmission among individuals. Similar to individual immune defenses, social immunity, that is antiparasite defenses mounted for the benefit of individuals other than the actor, is predicted to be altered in social groups. The eusocial honey bee (Apis mellifera) secretes glucose oxidase (GOX), an antiseptic enzyme, throughout its colony, thereby providing immune protection to other individuals in the hive. We conducted a laboratory experiment to investigate the effects of group density on social immunity, specifically GOX activity, body mass and feeding behavior in caged honey bees. Individual honeybees caged in a low group density displayed increased GOX activity relative to those kept at a high group density. In addition, we provided evidence for a trade‐off between GOX activity and body mass: Individuals caged in the low group density had a lower body mass, despite consuming more food overall. Our results provide the first experimental evidence that group density affects a social immune response in a eusocial insect. Moreover, we showed that the previously reported trade‐off between immunity and body mass extends to social immunity. GOX production appears to be costly for individuals, and potentially the colony, given that low body mass is correlated with small foraging ranges in bees. At high group densities, individuals can invest less in social immunity than at low densities, while presumably gaining shared protection from infection. Thus, there is evidence that trade‐offs at the individual level (GOX vs. body mass) can affect colony‐level fitness.

• Publication year

  2018

• Venue

  Ecology and Evolution

• Publication date

  2018-04-19

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1002/ece3.4011PMID 29876063PMCID 5980322
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Social immunity and the evolution of group living in insects

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• Social immunity of the family: parental contributions to a public good modulated by brood size

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• Effects of food quality on trade‐offs among growth, immunity and survival in the greater wax moth Galleria mellonella

  2015influential reference
• Parasitic and immune modulation of flight activity in honey bees tracked with optical counters

  2014cited by this paper
• Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys

  2014cited by this paper
• R: A language and environment for statistical computing.

  2014influential reference
• Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age

  2014cited by this paper
• Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects

  2013cited by this paper
• Integrating nutrition and immunology: a new frontier.

  2013cited by this paper
• Influence of Pollen Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter?

  2013cited by this paper
• Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity

  2012cited by this paper
• Social prophylaxis through distant corpse removal in ants

  2012cited by this paper
• Social context-dependent immune gene expression in bumblebees (Bombus terrestris)

  2012cited by this paper
• Sick ants become unsociable

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• Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees

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• Social Complexity and Nesting Habits Are Factors in the Evolution of Antimicrobial Defences in Wasps

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• Macronutrient balance mediates trade‐offs between immune function and life history traits

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• Antimicrobial strength increases with group size: implications for social evolution

  2011influential reference
• Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum.

  2011cited by this paper
• Diet effects on honeybee immunocompetence

  2010influential reference
• Nutritional regulation of division of labor in honey bees: toward a systems biology perspective

  2010cited by this paper
• Altruistic self‐removal of health‐compromised honey bee workers from their hive

  2010cited by this paper
• Moribund ants leave their nests to die in social isolation.

  2010cited by this paper
• The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.).

  2010cited by this paper
• Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus.

  2010cited by this paper
• The effects of age and social interactions on innate immunity in a leaf-cutting ant.

  2010cited by this paper
• Density-dependent prophylaxis in insects

  2009cited by this paper
• Rapid induction of immune density-dependent prophylaxis in adult social insects

  2009cited by this paper
• Social prophylaxis: group interaction promotes collective immunity in ant colonies.

  2007cited by this paper
• Diet-mediated effects of heavy metal pollution on growth and immune response in the geometrid moth Epirrita autumnata.

  2007influential reference
• Antimicrobial defences increase with sociality in bees

  2007cited by this paper
• Bee foraging ranges and their relationship to body size

  2007cited by this paper
• Effect of hydrogen peroxide on antibacterial activities of Canadian honeys.

  2006cited by this paper
• Inefficient task partitioning among nonhygienic honeybees, Apis mellifera L., and implications for disease transmission

  2006cited by this paper
• Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.).

  2005cited by this paper
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  2005cited by this paper
• An analysis of trade‐offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus

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  2005cited by this paper
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  2005cited by this paper
• Nutritional status influences socially regulated foraging ontogeny in honey bees

  2005cited by this paper
• Characterization of royal jelly proteins in both Africanized and European honeybees (Apis mellifera) by two-dimensional gel electrophoresis.

  2004cited by this paper
• The influence of different diets on haemocytes of adult worker honey bees, Apis mellifera

  2003cited by this paper
• Trade-offs in group living: transmission and disease resistance in leaf-cutting ants

  2002cited by this paper
• The development of immunity in a social insect: Evidence for the group facilitation of disease resistance

  2002cited by this paper
• Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.)

  2000cited by this paper
• Fever in honeybee colonies

  2000cited by this paper
• Quantification of Hemolymph Proteins as a Fast Method for Testing Protein Diets for Honey Bees (Hymenoptera: Apidae)

  1998cited by this paper
• Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae)

  1998cited by this paper
• Parasites and social insects

  1995cited by this paper
• Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function

  1992cited by this paper
• Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor.

  1992cited by this paper
• The protein balance of the honey bee worker.

  1990cited by this paper
• Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L.)

  1989cited by this paper
• Honey Bee Nutrition

  1969influential reference
• Effect of the Age of Pollen Used in Pollen Supplements on Their Nutritive Value for the Honeybee. I. Effect on Thoracic Weight, Development of Hypopharyngeal Glands, and Brood Rearing

  1968cited by this paper
• The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system.

  1963cited by this paper
• Protein and amino acid requirements of the honeybee (Apis mellifica L.)

  1953cited by this paper

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