, Volume 50, Issue 5, pp 704–719 | Cite as

The impacts of maternal stress on worker phenotypes in the honey bee

  • Sarah R. Preston
  • Joseph H. Palmer
  • James W. Harrison
  • Hanna M. Carr
  • Clare C. RittschofEmail author
Original article


Maternal stress is a common source of heritable health and behavioral variation. This type of maternal effect could be particularly important for honey bees (Apis mellifera), as a single queen is responsible for many generations of workers who perform all colony functions including raising subsequent worker generations. Multiple factors work synergistically to cause colony loss, but a role for maternal stress effects is unstudied. We used an artificial cold temperature treatment as a proof-of-concept approach to investigate whether acute queen stress causes changes in worker phenotypes, including egg hatching rate, development time, and adult behavior and immune function. We found that queen stress impacts early-life phenotypes (egg hatching and development time), with more limited impacts on adult phenotypes (behavior and immune function). Thus, if maternal stress impacts colony health, it is likely through cumulative impacts on worker population numbers, not through phenotypic effects that impact individual adult worker behavior or health resilience. This study addresses an important and overlooked question, and provides a baseline understanding of the likely impacts of queen stress on worker phenotypes.


maternal effects climate change queen failure immune function gene expression 


Authors’ contributions

S.R.P. carried out data collection, analysis, and manuscript writing. J.W.H. assisted in experimental setup and data collection. J.H.P. and H.M.C. conducted molecular analyses C.C.R. designed study, performed data analysis, and wrote manuscript.

Funding information

This work is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture Hatch Program under accession number 1012993, by a Foundation for Food and Agricultural Research Pollinator Health Fund (Grant ID: 549049), and by the University of Kentucky Bucks for Brains Summer Research Program.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2019_680_MOESM1_ESM.pdf (278 kb)
ESM 1. (PDF 277 kb)


  1. Alaux, C., Sinha, S., Hasadsri, L., Hunt, G.J., Guzman-Novoa, E., Degrandi-Hoffman, G., Uribe-Rubio, J.L., Southey, B.R., Rodriguez-Zas, S. & Robinson, G.E. (2009) Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc. Natl. Acad. Sci. U. S. A. 106, 15400–5.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alaux, C., Folschweiller, M., McDonnell, C., Beslay, D., Cousin, M., Dussaubat, C., Brunet, J.L. & Le Conte, Y. (2011) Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). J. Invertebr. Pathol. 106, 380–5.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Al-Lawati, H. & Bienefeld, K. (2009) Maternal Age Effects on Embryo Mortality and Juvenile Development of Offspring in the Honey Bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 102, 881–8.CrossRefGoogle Scholar
  4. Amdam, G.V. & Omholt, S.W. (2002) The Regulatory Anatomy of Honeybee Lifespan. J. Theor. Biol. 216, 209–28.CrossRefGoogle Scholar
  5. Amiri, E., Strand, M.K., Rueppell, O. & Tarpy, D.R. (2017) Queen Quality and the Impact of Honey Bee Diseases on Queen Health: Potential for Interactions between Two Major Threats to Colony Health. Insects 8, 48.PubMedCentralCrossRefGoogle Scholar
  6. Baer, B., Collins, J., Maalaps, K. & Boer, S.P.A. (2016) Sperm use economy of honeybee (Apis mellifera) queens. Ecol. Evol. 6, 2877–85.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barron, A.B. (2015) Death of the bee hive: Understanding the failure of an insect society. Curr. Opin. Insect Sci. 10, 45–50.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bates, B., Maechler, M., Bolker, B. & Walker, S. (2015) Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48.CrossRefGoogle Scholar
  9. Bonduriansky, R., Crean, A.J. & Day, T. (2012) The implications of nongenetic inheritance for evolution in changing environments. Evol. Appl. 5, 192–201.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Breed, M.D., Guzman-Novoa, E. & Hunt, G.J. (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 49, 271–98.PubMedCrossRefPubMedCentralGoogle Scholar
  11. Camazine, S.M. (1986) Differential reproduction of the mite, Varroa jacobsoni (Mesostigmata: Varroidae), on Africanized and European honey bees (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 79, 801–3.CrossRefGoogle Scholar
  12. Chaimanee, V., Evans, J.D., Chen, Y., Jackson, C. & Pettis, J.S. (2016) Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. J. Insect Physiol. 89, 1–8.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Collins, A.M. & Mazur, P. (2006) Chill sensitivity of honey bee, Apis mellifera, embryos. Cryobiology 53, 22–7.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Crino, O.L., Johnson, E.E., Blickley, J.L., Patricelli, G.L. & Breuner, C.W. (2013) The effects of experimentally elevated traffic noise on nestling white-crowned sparrow stress physiology, immune function, and life-history. J. Exp. Biol.Google Scholar
  15. DeGrandi-Hoffman, G., Chen, Y. & Simonds, R. (2013) The Effects of Pesticides on Queen Rearing and Virus Titers in Honey Bees (Apis mellifera L.). Insects 4, 71–89.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G. & Pennacchio, F. (2013) Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. U. S. A. 110, 18466–71.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Diss, A.L., J. G. Kunkel, M. E. Montgomery, D. E. Leonard (1996) Effects of maternal nutrition and egg provisioning on parameters of larval hatch, survival and dispersal in the gypsy moth, Lymantria dispar L. Oecologia 106, 470–7.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Doublet, V., Poeschl, Y., Gogol-Doring, A., Alaux, C., Annoscia, D., et al. (2017) Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens. BMC Genomics 18, 207.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dussaubat, C., Maisonnasse, A., Crauser, D., Tchamitchian, S., Bonnet, M., Cousin, M., Kretzschmar, A., Brunet, J.-L. & Le Conte, Y. (2016) Combined neonicotinoid pesticide and parasite stress alter honeybee queens’ physiology and survival. Sci. Rep. 6, 31430.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Kanost, M., Thompson, G.J., Zou, Z. & Hultmark, D. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–56.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Foray, V., Pelisson, P.-F., Bel-Venner, M.-C., Desouhant, E., Venner, S., Menu, F., Giron, D. & Rey, B. (2012) A handbook for uncovering the complete energetic budget in insects: the van Handel’s method (1985) revisited. Physiol. Entomol. 37, 295–302.CrossRefGoogle Scholar
  22. Forcada, J. & Hoffman, J.I. (2014) Climate change selects for heterozygosity in a declining fur seal population. Nature 511, 462.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fox, C.W. & Dingle, H. (1994) Dietary mediation of maternal age effects on offspring performance in a seed beetle (Coleoptera: Bruchidae). Funct. Ecol. 8, 600–6.CrossRefGoogle Scholar
  24. Fox, C.W., Thakar, M.S. & Mousseau, T.A. (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am. Nat. 149, 149–63.CrossRefGoogle Scholar
  25. Gibbs, M., Breuker, C.J., Hesketh, H., Hails, R.S. & Van Dyck, H. (2010) Maternal effects, flight versus fecundity trade-offs, and offspring immune defence in the Speckled Wood butterfly, Pararge aegeria. BMC Evol. Biol. 10, 345.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Goulson, D., Nicholls, E., Botias, C. & Rotheray, E.L. (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.CrossRefGoogle Scholar
  27. Graham, J.M. (2015) The Hive and the Honey Bee. Dadant & Sons, Hamilton, Illinois.Google Scholar
  28. Groh, C., Tautz, J. & Rossler, W. (2004) Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proc Natl. Acad. Sci. U. S. A. 101, 4268–73.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., et al. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12, e0185809.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Harrison, X.A., Donaldson, L., Correa-Cano, M.E., Evans, J., Fisher, D.N., Goodwin, C.E.D., Robinson, B.S., Hodgson, D.J. & Inger, R. (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6, e4794.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Jeffs, C.T. & Leather, S.R. (2014) Effects of extreme, fluctuating temperature events on life history traits of the grain aphid, Sitobion avenae. Entomol. Exp. Appl. 150, 240–9.CrossRefGoogle Scholar
  32. Johnson, R.M. (2015) Honey Bee Toxicology. Annu. Rev. Entomol. 60, 415–34.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Johnson, R.M., Pollock, H.S. & Berenbaum, M.R. (2009) Synergistic interactions between in-hive miticides in Apis mellifera. J. Econ. Entomol. 102, 474–9.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Keiser, C.N. & Mondor, E.B. (2013) Transgenerational Behavioral Plasticity in a Parthenogenetic Insect in Response to Increased Predation Risk. J. Insect Behav. 26, 603–13.CrossRefGoogle Scholar
  35. Khoury, D.S., Myerscough, M.R. & Barron, A.B. (2011) A quantitative model of honey bee colony population dynamics. PLoS One 6, e18491.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Klein, S., Cabirol, A., Devaud, J.-M., Barron, A.B. & Lihoreau, M. (2017) Why Bees Are So Vulnerable to Environmental Stressors. Trends Ecol. Evol. 32, 268–78.PubMedCrossRefPubMedCentralGoogle Scholar
  37. Lacour, G., Vernichon, F., Cadilhac, N., Boyer, S., Lagneau, C. & Hance, T. (2014) When mothers anticipate: Effects of the prediapause stage on embryo development time and of maternal photoperiod on eggs of a temperate and a tropical strains of Aedes albopictus (Diptera: Culicidae). J. Insect Physiol. 71, 87–96.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Li-Byarlay, H., Rittschof, C.C., Massey, J.H., Pittendrigh, B.R. & Robinson, G.E. (2014) Socially responsive effects of brain oxidative metabolism on aggression. Proc. Natl. Acad. Sci. U. S. A. 111, 12533–7.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Liess, M., Foit, K., Knillmann, S., Schafer, R.B. & Liess, H.D. (2016) Predicting the synergy of multiple stress effects. Sci. Rep. 6, 32965.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Lister, B.C. & Garcia, A. (2018) Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl. Acad. Sci. U. S. A. 115, E10397-E406.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Mackensen, O. (1951) Viability and sex determination in the honey bee (Apis mellifera L.). Genetics 36, 500–9.PubMedPubMedCentralGoogle Scholar
  42. Manley, R., Boots, M. & Wilfert, L. (2015) REVIEW: Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. J. Appl. Ecol. 52, 331–40.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Marshall, D.J. & Uller, T. (2007) When is a maternal effect adaptive? Oikos 116, 1957–63.CrossRefGoogle Scholar
  44. McIntyre, G.S. & Gooding, R.H. (2000) Egg size, contents, and quality: maternal-age and -size effects on house fly eggs. Can. J. Zool. 78, 1544–51.CrossRefGoogle Scholar
  45. McMahon, D.P., Natsopoulou, M.E., Doublet, V., Furst, M., Weging, S., Brown, M.J., Gogol-Doring, A. & Paxton, R.J. (2016) Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. Biol. Sci. 283.Google Scholar
  46. McMenamin, A.J. & Genersch, E. (2015) Honey bee colony losses and associated viruses. Curr. Opin. Insect Sci. 8.Google Scholar
  47. Mirth, C.K. & Riddiford, L.M. (2007) Size assessment and growth control: how adult size is determined in insects. Bioessays 29, 344–55.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Naeger, N.L., Van Nest, B.N., Johnson, J.N., Boyd, S.D., Southey, B.R., Rodriguez-Zas, S.L., Moore, D. & Robinson, G.E. (2011) Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees. J. Exp. Biol. 214, 979–87.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Nunes, F.M., Ihle, K.E., Mutti, N.S., Simoes, Z.L.P. & Amdam, G.V. (2013) The gene vitellogenin affects microRNA regulation in honey bee (Apis mellifera) fat body and brain. J. Exp. Biol. 216, 3724–32.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Pechenik, J.A. (2006) Larval experience and latent effects--metamorphosis is not a new beginning. Integr. Comp. Biol. 46, 323–33.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Perez-Sato, J.A., Kärcher, M.H., Hughes, W.O.H. & Ratnieks, F.L.W. (2015) Direct introduction of mated and virgin queens using smoke: a method that gives almost 100% acceptance when hives have been queenless for 2 days or more. J. Apic. Res. 47, 243–50.CrossRefGoogle Scholar
  52. Perry, C.J., Sovik, E., Myerscough, M.R. & Barron, A.B. (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl. Acad. Sci. U. S. A. 112, 3427–32.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Pettis, J.S., Rice, N., Joselow, K., vanEngelsdorp, D. & Chaimanee, V. (2016) Colony Failure Linked to Low Sperm Viability in Honey Bee (Apis mellifera) Queens and an Exploration of Potential Causative Factors. PLoS One 11, e0147220.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Räsänen, K. & Kruuk, L.E. (2007) Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21, 408–21.CrossRefGoogle Scholar
  55. Richard, F.-J., Holt, H.L. & Grozinger, C.M. (2012) Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 13, 558.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Rinderer, T.E. (2008) Bee Genetics and Breeding. Northern Bee Books.Google Scholar
  57. Rittschof, C.C. (2017) Sequential social experiences interact to modulate aggression but not brain gene expression in the honey bee (Apis mellifera). Front. Zool. 14, 1–10.CrossRefGoogle Scholar
  58. Rittschof, C.C. & Robinson, G.E. (2013) Manipulation of colony environment modulates honey bee aggression and brain gene expression. Genes Brain Behav. 12, 802–11.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Rittschof, C.C., Coombs, C.B., Frazier, M., Grozinger, C.M. & Robinson, G.E. (2015) Early-life experience affects honey bee aggression and resilience to immune challenge. Sci. Rep. 5, 15572.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Rittschof, C.C., Vekaria, H.J., Palmer, J.H. & Sullivan, P.G. (2018) Brain mitochondrial bioenergetics change with rapid and prolonged shifts in aggression in the honey bee, Apis mellifera. J. Exp. Biol. 221.Google Scholar
  61. Robinson, G.E. (1987) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 160, 613–9.CrossRefGoogle Scholar
  62. Sagili, R.R., Metz, B.N., Lucas, H.M., Chakrabarti, P. & Breece, C.R. (2018) Honey bees consider larval nutritional status rather than genetic relatedness when selecting larvae for emergency queen rearing. Sci. Rep. 8, 7679.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Salmela, H., Amdam, G.V. & Freitak, D. (2015) Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. PLoS Pathog. 11, e1005015.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to imageJ: 25 years of image analysis. Nat. Methods 9, 671–5.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Scofield, H.N. & Mattila, H.R. (2015) Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS One 10, e0121731.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Sheriff, M.J. & Love, O.P. (2013) Determining the adaptive potential of maternal stress. Ecol. Lett. 16, 271–80.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Smith, K.M., Loh, E.H., Rostal, M.K., Zambrana-Torrelio, C.M., Mendiola, L. & Daszak, P. (2013) Pathogens, pests, and economics: drivers of honey bee colony declines and losses. Ecohealth 10, 434–45.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Strasser, E.H. & Heath, J.A. (2013) Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J. Appl. Ecol. 50, 912–9.CrossRefGoogle Scholar
  69. Sulmon, C., van Baaren, J., Cabello-Hurtado, F., Gouesbet, G., Hennion, F., et al. (2015) Abiotic stressors and stress responses: What commonalities appear between species across biological organization levels? Environ. Pollut. 202, 66–77.PubMedCrossRefPubMedCentralGoogle Scholar
  70. Tarpy, D.R., Keller, J.J., Caren, J.R. & Delaney, D.A. (2012) Assessing the Mating ‘Health’ of Commercial Honey Bee Queens. J. Econ. Entomol. 105, 20–5.PubMedCrossRefPubMedCentralGoogle Scholar
  71. Team, R.C. (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  72. Tosi, S., Nieh, J.C., Sgolastra, F., Cabbri, R. & Medrzycki, P. (2017) Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. Biol. Sci. 284.Google Scholar
  73. Traynor, K.S., Wang, Y., Brent, C.S., Amdam, G.V. & Page, R.E. (2017) Young and old honeybee (Apis mellifera) larvae differentially prime the developmental maturation of their caregivers. Anim. Behav. 124, 193–202.CrossRefGoogle Scholar
  74. Walton, A. & Toth, A.L. (2016) Variation in individual worker honey bee behavior shows hallmarks of personality. Behav. Ecol. Sociobiol. 70, 999–1010.CrossRefGoogle Scholar
  75. Wang, Y., Kaftanoglu, O., Brent, C.S., Page, R.E. & Amdam, G.V. (2016) Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.). J. Exp. Biol. 219, 949.PubMedCrossRefPubMedCentralGoogle Scholar
  76. Wegener, J., Lorenz, M.W. & Bienefeld, K. (2010) Differences between queen- and worker-laid male eggs of the honey bee (Apis mellifera). Apidologie 41, 116–26.CrossRefGoogle Scholar
  77. Wilson-Rich, N., Dres, S.T. & Starks, P.T. (2008) The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera). J. Insect Physiol. 54, 1392–9.PubMedCrossRefPubMedCentralGoogle Scholar
  78. Winston, M.L. (1987) The Biology of the Honey Bee. In: (p. 47. Harvard University Press.Google Scholar
  79. Wolf, J.B. & Wade, M.J. (2009) What are maternal effects (and what are they not)? Philos. Trans. R. Soc. B 364, 1107–15.CrossRefGoogle Scholar
  80. Wray, M.K., Mattila, H.R. & Seeley, T.D. (2011) Collective personalities in honeybee colonies are linked to colony fitness. Anim. Behav. 81, 559–68.CrossRefGoogle Scholar
  81. Yu, R. & Omholt, S.W. (1999) Early developmental processes in the fertilised honeybee (Apis mellifera) oocyte. J. Insect Physiol. 45, 763–7.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Entomology, College of Agriculture, Food, and EnvironmentUniversity of KentuckyLexingtonUSA
  2. 2.College of Agriculture, Communities, and the EnvironmentKentucky State UniversityFrankfortUSA

Personalised recommendations