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Impact of Food Availability, Pathogen Exposure, and Genetic Diversity on Thermoregulation in Honey Bees (Apis mellifera)

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Abstract

Accurate thermoregulation in honey bees is crucial for colony survival. Multiple factors influence how colonies manage in-hive temperature, including genetic diversity. We explored the influence of genetic diversity on thermoregulatory behavior under three conditions: natural foraging, supplemental feeding, and exposure to the fungal pathogen shown to induce a social fever in honey bees. Our data suggest that (1) the degree of genetic diversity expected under normal conditions is not predictive of thermoregulatory stability, (2) the social fever response of honey bees is not a simple stimulus–response mechanism but appears to be influenced by ambient temperature conditions, and (3) a temperature-based circadian rhythm emerges under high nectar flow conditions. Taken together, these data suggest that a richer, context-dependent thermoregulatory system exists in honey bees than previously understood.

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References

  • Aronstein KA, Murray KD (2010) Chalkbrood disease in honey bees. J Invertebr Pathol 103:S20–S29

    Article  PubMed  Google Scholar 

  • Bailey L (1981) Honey bee pathology. Academic, London

    Google Scholar 

  • Bailey L, Ball BV (1991) Honey bee pathology. Academic, London

    Google Scholar 

  • Basile R (2009) Thermoregulation and resource management in the honeybee (Apis mellifera). Ph.D. Dissertation. University of Wurzburg, Germany

  • Basile R, Pirk CWW, Tautz J (2008) Trophallactic activities in the honeybee brood nest–heaters get supplied with high performance fuel. Zoology 111:433–441

    Article  PubMed  Google Scholar 

  • Chorbinski P, Rypula K (2003) Studies on the morphology of strains Ascosphaera apis isolated from chalkbrood disease of the honey bees. Vet Med 6:1–12

    Google Scholar 

  • Delaney DA, Keller JJ, Caren JR, Tarpy DR (2011) The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera). Apidologie 42:1–13

    Article  Google Scholar 

  • Eban-Rothschild A, Bloch G (2012) Circadian rhythms and sleep in honey bees. In: Galizia GC, Eisenhardt D, Giurfa M (eds). Honeybee neurobiology and behavior: a tribute to Randolf Menzel. Springer, Dordrecht, The Netherlands, pp 31–46

  • Edery I (2000) Circadian rhythms in a nutshell. Physiol Genomics 3:59–74

    CAS  PubMed  Google Scholar 

  • Evans JD, Spivak M (2010) Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 103:S62–S72

    Article  PubMed  Google Scholar 

  • Flores JM, Ruiz JA, Ruz JM, Puerta F, Bustos M, Padilla F, Campano F (1996) Effect of temperature and humidity of sealed brood on chalkbrood development under controlled conditions. Apidologie 27:185–192

    Article  Google Scholar 

  • Flores JM, Gutierrez I, Puerta F (2004) A comparison of methods to experimentally induce chalk brood disease in honey bees. Span J Agric Res 2:79–83

    Google Scholar 

  • Frisch B, Aschoff J (1987) Circadian rhythms in honeybees: entrainment by feeding cycles. Physiol Entomol 12:41–49

    Article  Google Scholar 

  • Fuchs S, Moritz RFA (1998) Evolution of extreme polyandry in the honeybee Apis mellifera L. Behav Ecol Sociobiol 9:269–275

    Google Scholar 

  • Fuller P, Lu J, Saper C (2008) Differential rescue of light- and food- entrainable circadian rhythms. Science 320:1074–1077

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gates B (1914) The temperature of the bee colony. Bull US Dep Agric 96:1–29

    Google Scholar 

  • Graham S, Myerscough MR, Jones JC, Oldroyd BP (2006) Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis mellifera L.) colonies. Insect Soc 53:226–232

    Article  Google Scholar 

  • 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 101:4268–4273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hou C, Kaspari M, Vander Zanden H, Gillooly J (2010) Energetic basis of colonial living in social insects. Biol Lett 107:3634–3638

    CAS  Google Scholar 

  • Humphrey JAC, Dykes ES (2008) Thermal energy conduction in a honey bee comb due to cell-heating bees. J Theor Biol 250:194–208

    Article  CAS  PubMed  Google Scholar 

  • Jones J, Oldroyd B (2007) Nest thermoregulation in social insects. Adv Insect Physiol 33:153–191

    Article  Google Scholar 

  • Jones J, Myerscough M, Graham S, Oldroyd B (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404

    Article  CAS  PubMed  Google Scholar 

  • Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste-dependent sleep of worker honey bees. J Exp Biol 211:3028–3040

    Article  PubMed  Google Scholar 

  • Kleinhenz M, Bujok B, Fuchs S, Tautz J (2003) Hot bees in empty broodnest cells: heating from within. J Exp Biol 206(23):4217–4231

    Article  PubMed  Google Scholar 

  • Kraus FB, Neumann P, van Praagh J, Moritz RFA (2004) Sperm limitation and the evolution of polyandry in the honeybee (Apis mellifera L.). Behav Ecol Sociobiol 55:494–501

    Article  Google Scholar 

  • Kronenberg F, Heller C (1982) Colonial thermoregulation in honey bees (Apis mellifera). J Comp Physiol B 148:65–76

    Article  Google Scholar 

  • Mattila H, Seeley T (2007) Genetic diversity in honey bee colonies enhances productivity. Science 317:362–364

    Article  CAS  PubMed  Google Scholar 

  • Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 8:843–857

    Article  Google Scholar 

  • Moore D, Rankin MA (1993) Light and temperature entrainment of a locomotor rhythm in honeybees. Physiol Entomol 18:271–278

    Article  Google Scholar 

  • Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164

    Article  PubMed  Google Scholar 

  • Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413

    Article  PubMed  Google Scholar 

  • Page R (1980) The evolution of multiple mating behavior by honey bee queens (Apis Mellifera L.). Genetics 96:263–273

    PubMed Central  PubMed  Google Scholar 

  • Page RE, Robinson GE, Calderone NE, Rothenbuhler WC (1989) Genetic structure, division of labor, and the evolution of insect societies. In: Breed MD, Page RE (eds) The genetics of social evolution. Westview, Boulder, pp 15–30

    Google Scholar 

  • Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera). Behav Ecol Sociobiol 36:387–396

    Article  Google Scholar 

  • Palmer K, Oldroyd B (2000) Evolution of multiple mating in the genus Apis. Apidologie 31:235–248

    Article  Google Scholar 

  • Pratt SC (2004) Collective control of the timing and type of comb construction by honey bees (Apis mellifera). Apidologie 35:193–205

    Article  Google Scholar 

  • Robinson G, Page R (1989) Genetic basis for division of labour in an insect society. In: The genetics of social evolution. Westview Press, Boulder, pp 61–88

    Google Scholar 

  • Rueppell O, Johnson N, Rychtar J (2008) Variance-based selection may explain general mating patterns in social insects. Biol Lett 4:270–273

    Article  PubMed Central  PubMed  Google Scholar 

  • Seeley TD (1985) Honeybee ecology: a study of adaptation in social life. Princeton Univ. Press, Princeton

    Google Scholar 

  • Seeley TD (1995) The wisdom of the hive. Harvard University Press, Cambridge

    Google Scholar 

  • Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc 274:67–72

    Article  Google Scholar 

  • Sherman PW, Seeley TD, Reeve HK (1998) Parasites, pathogens, and polyandry in social hymenoptera. Am Nat 131:602–610

    Article  Google Scholar 

  • Siegel AJ, Hui J, Johnson RN, Starks PT (2005) Mobile insulator units: honey bee workers as living insulation. Insect Soc 52:242–246

    Article  Google Scholar 

  • Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9:735–748

    Article  CAS  PubMed  Google Scholar 

  • Solignac M, Vautrin D, Loiseau A, Mougel F, Baudry E, Estoup A, Garnery L, Haberl M, Cornuet J-M (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Molec Ecol Notes 3:307–311

    Google Scholar 

  • Southwick E (1982) Metabolic energy of intact honey bee colonies. Comp Biochem Physiol 71:277–281

    Article  Google Scholar 

  • Southwick EE (1987) Cooperative metabolism in honey bees: an alternative to antifreeze and hibernation. J Therm Biol 12(2):155–158

    Article  Google Scholar 

  • Southwick EE, Heldmaier G (1987) Temperature control in honey bee colonies, precise social cooperation permits adaptation to temperate climates. Bioscience 37:395–399

    Article  Google Scholar 

  • Stabentheiner A, Kovac H, Brodschneider R (2010) Honeybee colony thermoregulation–regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress. PLoS ONE 5(1). doi:10.1371/journal.pone.0008967

  • Starks PT, Blackie CA, Seeley TD (2000) Fever in honeybee colonies. Naturwissenschaften 87:229–231

    Article  CAS  PubMed  Google Scholar 

  • Starks PT, Johnson RN, Siegel AJ, Decelle MM (2005) Heat-shielding: a task for youngsters. Behav Ecol 16:128–132

    Article  Google Scholar 

  • Swanson JAI, Torto B, Kells SA, Mesce KA, Tumlinson JH, Spivak M (2009) Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J Chem Ecol 35:1108–1116

    Article  CAS  PubMed  Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc B 270:99–103

    Article  PubMed Central  PubMed  Google Scholar 

  • Tarpy DR, Nielsen D (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera: Apidae). Ann Entomol Soc Am 95:513–528

    Article  Google Scholar 

  • Tarpy DR, Nielsen R, Nielsen DI (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insect Soc 51:203–204

    Article  Google Scholar 

  • Tarpy DR, Caren J, Delaney D, Sammataro D, Finley J, Loper G et al (2010) Mating frequencies of Africanized honey bees in the South Western USA. J Apic Res 49:302–310

    Article  Google Scholar 

  • Tarpy DR, vanEngelsdorp D, Pettis JS (2013) Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften 100:723–728

    Article  CAS  PubMed  Google Scholar 

  • Tautz J, Maier S, Rossler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. Proc Natl Acad Sci 100:7343–7347

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vojvodic S, Jensen AB, James RR, Boomsma JJ, Eilenberg J (2011) Temperature dependent virulence of obligate and facultative fungal pathogens of honeybee brood. Vet Microbiol 149:200–205

    Article  CAS  PubMed  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex(r) 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTech 10:506–513

    CAS  Google Scholar 

  • Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423

    Article  CAS  PubMed  Google Scholar 

  • Wilson-Rich N, Tarpy DR, Starks PT (2012) Within- and across-colony effects of hyperpolyandry on immune function and body condition in honey bees (Apis mellifera). J Insect Physiol 58:402–407

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Joel Caren for assisting with the genotyping of the colonies. This study was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2007-02281, and a National Science Foundation REU site award to Tufts University (DBI-0649190).

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Correspondence to P. T. Starks.

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Simone-Finstrom, M., Foo, B., Tarpy, D.R. et al. Impact of Food Availability, Pathogen Exposure, and Genetic Diversity on Thermoregulation in Honey Bees (Apis mellifera). J Insect Behav 27, 527–539 (2014). https://doi.org/10.1007/s10905-014-9447-3

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