Early-life experience affects honey bee aggression and resilience to immune challenge.

Clare C Rittschof, Chelsey B Coombs, Maryann Frazier, Christina M Grozinger, Gene E Robinson
Author Information
  1. Clare C Rittschof: Carl R. Woese Institute for Genomic Biology, Department of Entomology and Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, IL, 61801.
  2. Chelsey B Coombs: Department of Molecular and Cellular Biology, University of Illinois Urbana-Champaign, Urbana, IL, 61801.
  3. Maryann Frazier: Department of Entomology, Center for Pollinator Research, The Pennsylvania State University, University Park, PA, 16802.
  4. Christina M Grozinger: Department of Entomology, Center for Pollinator Research, The Pennsylvania State University, University Park, PA, 16802.
  5. Gene E Robinson: Carl R. Woese Institute for Genomic Biology, Department of Entomology and Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, IL, 61801.

Abstract

Early-life social experiences cause lasting changes in behavior and health for a variety of animals including humans, but it is not well understood how social information ''gets under the skin'' resulting in these effects. Adult honey bees (Apis mellifera) exhibit socially coordinated collective nest defense, providing a model for social modulation of aggressive behavior. Here we report for the first time that a honey bee's early-life social environment has lasting effects on individual aggression: bees that experienced high-aggression environments during pre-adult stages showed increased aggression when they reached adulthood relative to siblings that experienced low-aggression environments, even though all bees were kept in a common environment during adulthood. Unlike other animals including humans however, high-aggression honey bees were more, rather than less, resilient to immune challenge, assessed as neonicotinoid pesticide susceptibility. Moreover, aggression was negatively correlated with ectoparasitic mite presence. In honey bees, early-life social experience has broad effects, but increased aggression is decoupled from negative health outcomes. Because honey bees and humans share aspects of their physiological response to aggressive social encounters, our findings represent a step towards identifying ways to improve individual resiliency. Pre-adult social experience may be crucial to the health of the ecologically threatened honey bee.

References

  1. Annu Rev Neurosci. 2004;27:549-79 [PMID: 15217343]
  2. Trends Genet. 2004 Mar;20(3):163-70 [PMID: 15036810]
  3. Proc Natl Acad Sci U S A. 2005 May 24;102(21):7470-5 [PMID: 15897457]
  4. Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):17929-34 [PMID: 25453090]
  5. Proc Natl Acad Sci U S A. 2014 Aug 26;111(34):12533-7 [PMID: 25092297]
  6. J Chem Ecol. 2007 Jul;33(7):1346-50 [PMID: 17505874]
  7. JAMA Psychiatry. 2013 Apr;70(4):419-26 [PMID: 23426798]
  8. Genes Brain Behav. 2015 Feb;14(2):158-66 [PMID: 25640316]
  9. BMC Genomics. 2014 Jan 28;15:75 [PMID: 24472515]
  10. Mol Genet Genomics. 2001 Dec;266(4):556-63 [PMID: 11810226]
  11. Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):18020-5 [PMID: 21960440]
  12. Genetics. 1998 Mar;148(3):1203-13 [PMID: 9539435]
  13. Proc Biol Sci. 2007 Jun 22;274(1617):1517-21 [PMID: 17439851]
  14. Neotrop Entomol. 2007 Nov-Dec;36(6):949-52 [PMID: 18246271]
  15. Nature. 2011 May 26;473(7348):478-83 [PMID: 21516106]
  16. Nat Cell Biol. 2011 Aug 28;13(10):1272-9 [PMID: 21968997]
  17. BMC Genomics. 2012 Oct 16;13:558 [PMID: 23072398]
  18. Proc Natl Acad Sci U S A. 2004 Mar 23;101(12):4268-73 [PMID: 15024125]
  19. Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14716-21 [PMID: 19617551]
  20. Adv Genet. 2012;77:33-57 [PMID: 22902125]
  21. Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1920-5 [PMID: 12578963]
  22. Genes Brain Behav. 2013 Nov;12(8):802-11 [PMID: 24034579]
  23. Science. 1997 Sep 12;277(5332):1659-62 [PMID: 9287218]
  24. J Evol Biol. 2011 Sep;24(9):1939-48 [PMID: 21696476]
  25. Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18466-71 [PMID: 24145453]
  26. BMC Genomics. 2013 Dec 19;14:903 [PMID: 24350621]
  27. PLoS One. 2013 Oct 10;8(10):e77354 [PMID: 24130876]
  28. J Comp Neurol. 1999 Nov 8;414(1):97-113 [PMID: 10494081]
  29. Anim Behav. 1998 Jan;55(1):13-20 [PMID: 9480667]
  30. Anim Behav. 1999 Sep;58(3):621-628 [PMID: 10479377]
  31. Am J Prev Med. 1998 May;14(4):245-58 [PMID: 9635069]
  32. Proc Natl Acad Sci U S A. 2011 Aug 2;108(31):12657-62 [PMID: 21775671]
  33. Parasitology. 2007 Mar;134(Pt 3):405-12 [PMID: 17078903]
  34. Bioessays. 2007 Feb;29(2):133-44 [PMID: 17226801]
  35. Biol Psychiatry. 2008 Aug 15;64(4):266-72 [PMID: 18440494]
  36. J Virol Methods. 2007 Apr;141(1):7-13 [PMID: 17166598]
  37. Trends Pharmacol Sci. 2011 Dec;32(12):708-14 [PMID: 21975165]
  38. Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5657-63 [PMID: 18408154]
  39. Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15400-5 [PMID: 19706434]
  40. Proc Natl Acad Sci U S A. 2013 May 28;110(22):8842-6 [PMID: 23630255]
  41. PLoS One. 2015 Apr 08;10(4):e0121731 [PMID: 25853902]

MeSH Term

Aggression
Animals
Bees
Behavior, Animal

Word Cloud

Created with Highcharts 10.0.0socialhoneybeesaggressionhealthhumanseffectsexperienceEarly-lifelastingbehavioranimalsincludingaggressiveearly-lifeenvironmentindividualexperiencedhigh-aggressionenvironmentsincreasedadulthoodimmunechallengebeeexperiencescausechangesvarietywellunderstoodinformation''getsskin''resultingAdultApismelliferaexhibitsociallycoordinatedcollectivenestdefenseprovidingmodelmodulationreportfirsttimebee'saggression:pre-adultstagesshowedreachedrelativesiblingslow-aggressioneventhoughkeptcommonUnlikehoweverratherlessresilientassessedneonicotinoidpesticidesusceptibilityMoreovernegativelycorrelatedectoparasiticmitepresencebroaddecouplednegativeoutcomesshareaspectsphysiologicalresponseencountersfindingsrepresentsteptowardsidentifyingwaysimproveresiliencyPre-adultmaycrucialecologicallythreatenedaffectsresilience

Similar Articles

Cited By