Skip to main content
SpringerLink
Log in

The architecture of the pollen hoarding syndrome in honey bees: implications for understanding social evolution, behavioral syndromes, and selective breeding

  • Review article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Social evolution has influenced every aspect of contemporary honey bee biology, but the details are difficult to reconstruct. The reproductive ground plan hypothesis of social evolution proposes that central regulators of the gonotropic cycle of solitary insects have been co-opted to coordinate social complexity in honey bees, such as the division of labor among workers. The predicted trait associations between reproductive physiology and social behavior have been identified in the context of the pollen hoarding syndrome, a larger suite of interrelated traits. The genetic architecture of this syndrome is characterized by a partially overlapping genetic architecture with several consistent, pleiotropic quantitative trait loci (QTL). Despite these central QTL and an integrated hormonal regulation, separate aspects of the pollen hoarding syndrome may evolve independently due to peripheral QTL and additionally segregating genetic variance. The characterization of the pollen hoarding syndrome has also demonstrated that this syndrome involves many non-behavioral traits, which may be the case for numerous “behavioral” syndromes. Furthermore, the genetic architecture of the pollen hoarding syndrome has implications for breeding programs for improving honey health and other desirable traits: if these traits are comparable to the pollen hoarding syndrome, consistent pleiotropic QTL will enable marker-assisted selection, while sufficient additional genetic variation may permit the dissociation of trade-offs for efficient multiple trait selection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agrawal, A.F., Stinchcombe, J.R. (2009) How much do genetic covariances alter the rate of adaptation? Proc. R. Soc. B-Biol. Sci. 276(1659), 1183–1191

    Article  Google Scholar 

  • Amdam, G.V., Csondes, A., Fondrk, M.K., Page, R.E. (2006a) Complex social behaviour derived from maternal reproductive traits. Nature 439, 76–78

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Amdam, G.V., Nilsen, K.A., Norberg, K., Fondrk, M.K., Hartfelder, K. (2007) Variation in endocrine signaling underlies variation in social life history. Am. Nat. 170(1), 37–46

    Article  PubMed Central  PubMed  Google Scholar 

  • Amdam, G.V., Norberg, K., Fondrk, M.K., Page, R.E. (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. U. S. A. 101(31), 11350–11355

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Amdam, G.V., Norberg, K., Hagen, A., Omholt, S.W. (2003) Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. U. S. A. 100(4), 1799–1802

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Amdam, G.V., Norberg, K., Page, R.E., Erber, J., Scheiner, R. (2006b) Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behav. Brain Res. 169(2), 201–205

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Amdam, G.V., Page, R.E. (2010) The developmental genetics and physiology of honeybee societies. Anim. Behav. 79(5), 973–980

    Article  PubMed Central  PubMed  Google Scholar 

  • Amdam, G.V., Page, R.E., Fondrk, M.K., Brent, C.S. (2010) Hormone response to bidirectional selection on social behavior. Evol. Dev. 12(5), 428–436

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Arechavaleta-Velasco, M.E., Alcala-Escamilla, K., Robles-Rios, C., Tsuruda, J.M., Hunt, G.J. (2012) Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS One 7(11), e47269

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Arias, M.C., Sheppard, W.S. (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol. Phylogenet. Evol. 37(1), 25–35

    Article  PubMed  CAS  Google Scholar 

  • Bailey, L., Ball, B.V. (1991) Honey Bee Pathology. Academic, London

    Google Scholar 

  • Behrens, D., Huang, Q., Gessner, C., Rosenkranz, P., Frey, E., Locke, B., Moritz, R.F., Kraus, F.B. (2011) Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecol. Evol. 1(4), 451–458

    Article  PubMed Central  PubMed  Google Scholar 

  • Bourgeois, A.L., Rinderer, T.E. (2009) Genetic characterization of Russian Honey Bee stock selected for improved resistance to Varroa destructor. J. Econ. Entomol. 102(3), 1233–1238

    Article  PubMed  CAS  Google Scholar 

  • Camazine, S. (1986) Differential reproduction of the mite, Varroa jacobsoni (Mesostigmata, Varroidae), on Africanized and European honey bees (Hymenoptera, Apidae). Ann. Entomol. Soc. Am. 79(5), 801–803

    Google Scholar 

  • Conner, J.K. (2003) Artificial selection: a powerful tool for ecologists. Ecology 84(7), 1650–1660

    Article  Google Scholar 

  • Delph, L.F., Arntz, A.M., Scotti-Saintagne, C., Scotti, I. (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64(10), 2873–2886

    PubMed  Google Scholar 

  • Dixon, L.R., McQuage, M.R., Lonon, E.J., Buehler, D., Seck, O., Rueppell, O. (2012) Pleiotropy of segregating genetic variants that affect honey bee worker life expectancy. Exp. Gerontol. 47(8), 631–637

    Article  PubMed Central  PubMed  Google Scholar 

  • Dreller, C., Page, R.E., Fondrk, M.K. (1999) Regulation of pollen foraging in honeybee colonies: effects of young brood, stored pollen, and empty space. Behav. Ecol. Sociobiol. 45, 227–233

    Article  Google Scholar 

  • Dreller, C., Tarpy, D.R. (2000) Perception of the pollen need by foragers in a honeybee colony. Anim. Behav. 59(1), 91–96

    Article  PubMed  Google Scholar 

  • Engel, M.S. (1998) Fossil honey bees and evolution in the genus Apis (Hymenoptera : Apidae). Apidologie 29(3), 265–281

    Article  Google Scholar 

  • Fewell, J.H., Page, R.E. (1993) Genotypic variation in foraging responses to environmental stimuli by honey bees, Apis mellifera. Experientia 49(12), 1106–1112

    Article  Google Scholar 

  • Fewell, J.H., Winston, M.L. (1992) Colony state and regulation of pollen foraging in the honey-bee, Apis mellifera L. Behav. Ecol. Sociobiol. 30, 387–393

    Article  Google Scholar 

  • Fewell, J.H., Winston, M.L. (1996) Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera. Behav. Ecol. 7(3), 286–291

    Article  Google Scholar 

  • Gadagkar, R. (1997) The evolution of caste polymorphism in social insects: genetic release followed by diversifying evolution. J. Genet. 76(3), 167–179

    Article  Google Scholar 

  • Goode, K., Huber, Z., Mesce, K.A., Spivak, M. (2006) Hygienic behavior of the honey bee (Apis mellifera) is independent of sucrose responsiveness and foraging ontogeny. Horm. Behav. 49(3), 391–397

    Article  PubMed  CAS  Google Scholar 

  • Graham, A.M., Munday, M.D., Kaftanoglu, O., Page, R.E., Amdam, G.V., Rueppell, O. (2011) Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol. Biol. 11, 95

    Article  PubMed Central  PubMed  Google Scholar 

  • Harris, J.W. (2007) Bees with Varroa sensitive hygiene preferentially remove mite infested pupae aged < = five days post capping. J. Apic. Res. 46(3), 134–139

    Article  Google Scholar 

  • Hellmich, R.L., Kulincevic, J.M., Rothenbuhler, W.C. (1985) Selection for high and low pollen-hoarding honey bees. J. Hered. 76(3), 155–158

    Google Scholar 

  • Holloway, B., Sylvester, H.A., Bourgeois, L., Rinderer, T.E. (2012) Association of single nucleotide polymorphisms to resistance to chalkbrood in Apis mellifera. J. Apic. Res. 51(2), 154–163

    Article  CAS  Google Scholar 

  • Huang, Q., Kryger, P., Le Conte, Y., Moritz, R.F. (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J. Invertebr. Pathol. 109(3), 297–302

    Article  PubMed  Google Scholar 

  • Humann, F.C., Hartfelder, K. (2011) Representational Difference Analysis (RDA) reveals differential expression of conserved as well as novel genes during caste-specific development of the honey bee (Apis mellifera L.) ovary. Insect Biochem. Mol. 41(8), 602–612

    Article  CAS  Google Scholar 

  • Humphries, M.A., Fondrk, M.K., Page, R.E. (2005) Locomotion and the pollen hoarding behavioral syndrome of the honeybee (Apis mellifera L.). J. Comp. Physiol. A. 191(7), 669–674

    Article  CAS  Google Scholar 

  • Humphries, M.A., Muller, U., Fondrk, M.K., Page, R.E. (2003) PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior. J. Comp. Physiol. A. 189(7), 555–562

    Article  CAS  Google Scholar 

  • Hunt, G.J., Amdam, G.V., Schlipalius, D., Emore, C., Sardesai, N., et al. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94(4), 247–267

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hunt, G.J., Page Jr., R.E., Fondrk, M.K., Dullum, C.J. (1995) Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141, 1537–1545

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ihle, K.E., Page, R.E., Frederick, K., Fondrk, M.K., Amdam, G.V. (2010) Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Anim. Behav. 79(5), 1001–1006

    Article  PubMed Central  PubMed  Google Scholar 

  • Jandt, J.M., Bengston, S. Pinter-Wollman, N. Pruitt, J.N., Raine, N.E., Dornhaus, A. Sih A. (2013) Behavioural syndromes and social insects: personality at multiple levels. Biol. Rev. Online. In press.

  • Kulincevic, J.M., Rothenbuhler, W.C. (1975) Selection for resistance and susceptibility to hairless-black syndrome in the honeybee. J. Invertebr. Pathol. 25(3), 289–295

    Article  PubMed  CAS  Google Scholar 

  • Laidlaw, H.H., Page, R.E. (1997) Queen rearing and bee breeding. Wicwas Press, Cheshire

    Google Scholar 

  • Lande, R. (1982) A quantitative genetic theory of life history evolution. Ecology 63(3), 607–615

    Article  Google Scholar 

  • Lande, R. (1984) The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. 44(3), 309–320

    PubMed  CAS  Google Scholar 

  • Lapidge, K.L., Oldroyd, B.P., Spivak, M. (2002) Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften 89(12), 565–568

    PubMed  CAS  Google Scholar 

  • Le Conte, Y., Alaux, C., Martin, J.F., Harbo, J.R., Harris, J.W., Dantec, C., Severac, D., Cros-Arteil, S., Navajas, M. (2011) Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour. Insect Mol. Biol. 20(3), 399–408

    Article  PubMed  Google Scholar 

  • Linksvayer, T.A., Fondrk, M.K., Page, R.E. (2009a) Honeybee social regulatory networks are shaped by colony-level selection. Am. Nat. 173(3), E99–E107

    Article  PubMed  Google Scholar 

  • Linksvayer, T.A., Rueppell, O., Siegel, A., Kaftanoglu, O., Page, R.E., Amdam, G.V. (2009b) The genetic basis of transgressive ovary size in honey bee workers. Genetics 183, 693–707

    Article  PubMed Central  PubMed  Google Scholar 

  • Mutti, N.S., Dolezal, A.G., Wolschin, F., Mutti, J.S., Gill, K.S., Amdam, G.V. (2011) IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J. Exp. Biol. 214(23), 3977–3984

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nelson, C.M., Ihle, K.E., Fondrk, M.K., Page, R.E., Amdam, G.V. (2007) The gene vitellogenin has multiple coordinating effects on social organization. Plos Biol. 5(3), e62

    Article  PubMed Central  PubMed  Google Scholar 

  • Nilsen, K.A., Ihle, K.E., Frederick, K., Fondrk, M.K., Smedal, B., Hartfelder, K., Amdam, G.V. (2011) Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. J. Exp. Biol. 214(9), 1488–1497

    Article  PubMed Central  PubMed  Google Scholar 

  • O'Hagan, S.J., Knowles, D.B., Kell (2012) Exploiting genomic knowledge in optimising molecular breeding programmes: algorithms from evolutionary computing. PLoS One 7(11). In press.

  • Oxley, P.R., Spivak, M., Oldroyd, B.P. (2010) Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19(7), 1452–1461

    Article  PubMed  CAS  Google Scholar 

  • Page, R.E., Amdam, G.V. (2007) The making of a social insect: developmental architectures of social design. Bioessays 29, 334–343

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Page, R.E., Erber, J. (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89, 91–106

    Article  PubMed  CAS  Google Scholar 

  • Page, R.E., Fondrk, M.K. (1995) The effects of colony level selection on the social organization of honey bee (Apis mellifera L) colonies - colony level components of pollen hoarding. Behav. Ecol. Sociobiol. 36(2), 135–144

    Article  Google Scholar 

  • Page, R.E., Fondrk, M.K., Hunt, G.J., Guzman-Novoa, E., Humphries, M.A., Nguyen, K., Greene, A.S. (2000) Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J Hered. 91(6), 474–479

    Article  PubMed  Google Scholar 

  • Page, R.E., Fondrk, M.K., Rueppell, O. (2012a) Complex pleiotropy characterizes the pollen hoarding syndrome in honey bees (Apis mellifera L.). Behav. Ecol. Sociobiol. 66(11), 1459–1466

    Article  PubMed Central  PubMed  Google Scholar 

  • Page, R.E., Rueppell, O., Amdam, G.V. (2012b) Genetics of reproduction and regulation of honeybee (Apis mellifera L.) social behavior. Annu. Rev. Genet. 46, 97–119

    Article  PubMed  CAS  Google Scholar 

  • Palmer, K.A., Oldroyd, B.P. (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90(6), 265–268

    Article  PubMed  CAS  Google Scholar 

  • Pankiw, T. (2003) Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.). Behav. Ecol. Sociobiol. 54(5), 458–464

    Article  Google Scholar 

  • Pankiw, T., Page, R.E. (2001) Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behav. Ecol. Sociobiol. 51, 87–94

    Article  Google Scholar 

  • Pianka, E.R. (1970) On r- and K-selection. Am. Nat. 104(940), 592–597

    Article  Google Scholar 

  • Price, T., Langen, T. (1992) Evolution of correlated characters. Trends Ecol. Evol. 7(9), 307–310

    Article  PubMed  CAS  Google Scholar 

  • Rinderer, T.E., Harris, J.W., Hunt, G.J., de Gusman, L.I. (2010) Breeding for resistance to Varroa destructor in North America. Apidologie 41(3), 409–424

    Article  Google Scholar 

  • Roff, D.A. (2011) Genomic insights into life history evolution. In: Flatt, T., Heyland, A. (eds.) Mechanisms of Life History Evolution, pp. 11–25. Oxford University Press, Oxford

    Chapter  Google Scholar 

  • Rueppell, O. (2009) Characterization of quantitative trait loci for the age of first foraging in honey bee workers. Behav. Genet. 39, 541–553

    Article  PubMed  Google Scholar 

  • Rueppell, O., Bachelier, C., Fondrk, M.K., Page, R.E. (2007) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42, 1020–1032

    Article  PubMed Central  PubMed  Google Scholar 

  • Rueppell, O., Chandra, S.B.C., Pankiw, T., Fondrk, M.K., Beye, M., Hunt, G.J., Page, R.E. (2006a) The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.). Genetics 172, 243–251

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rueppell, O., Fondrk, M.K., Page, R.E. (2006b) Male maturation response to selection of the pollen-hoarding syndrome in honey bees (Apis mellifera L.). Anim. Behav. 71, 227–234

    Article  PubMed Central  PubMed  Google Scholar 

  • Rueppell, O., Hunggims, E., Tingek, S. (2008) Association between larger ovaries and pollen foraging in queenless Apis cerana workers supports the reproductive ground-plan hypothesis of social evolution. J. Insect Behav. 21, 317–321

    Article  Google Scholar 

  • Rueppell, O., Metheny, J.D., Linksvayer, T.A., Fondrk, M.K., Page, R.E., Amdam, G.V. (2011) Genetic architecture of ovary size and asymmetry in European honeybee workers. Heredity 106, 894–903

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rueppell, O., Pankiw, T., Nielsen, D.I., Fondrk, M.K., Beye, M., Page, R.E. (2004) The genetic architecture of the behavioral ontogeny of foraging in honey bee workers. Genetics 167, 1767–1779

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rüppell, O., Pankiw, T., Nielson, D.I., Fondrk, M.K., Beye, M., Page, R.E. (2004) Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J. Hered. 95, 481–491

    Article  PubMed  Google Scholar 

  • Scheiner, R., Page, R.E., Erber, J. (2001) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol. Learn. Mem. 76(2), 138–150

    Article  PubMed  CAS  Google Scholar 

  • Schmid-Hempel, P. (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

  • Sih, A., Bell, A., Johnson, J.C. (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372–378

    Article  PubMed  Google Scholar 

  • Spivak, M., Gilliam, M. (1998) Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa Part I. Hygienic behaviour and resistance to American foulbrood. Bee World 79(3), 124–134. 169–186

    Google Scholar 

  • Spivak, M., Reuter, G.S., Lee, K., Ranum, B. (2009) The future of the MN hygienic stock of bees is in good hands! Am. Bee J. 149(10), 965–967

    Google Scholar 

  • Stearns, S.C. (1989) Trade-offs in life-history evolution. Funct. Ecol. 3(3), 259–268

    Article  Google Scholar 

  • Toth, A.L., Robinson, G.E. (2007) Evo-devo and the evolution of social behavior. Trends Genet. 23(7), 334–341

    Article  PubMed  CAS  Google Scholar 

  • Tsuruda, J.M., Harris, J.W., Bourgeois, L., Danka, R.G., Hunt, G.J. (2012) High-resolution linkage analyses to identify genes that influence Varroa sensitive hygiene behavior in honey bees. PLoS One 7(11)

  • Tsuruda, J.M., Page, R.E. (2009) The effects of foraging role and genotype on light and sucrose responsiveness in honey bees (Apis mellifera L.). Behav Brain Res. 205(1), 132–137

    Article  PubMed  CAS  Google Scholar 

  • vanEngelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., et al. (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4(8), e6481

    Article  PubMed Central  PubMed  Google Scholar 

  • vanEngelsdorp, D., Meixner, M.D. (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 103, S80–S95

    Article  PubMed  Google Scholar 

  • vanEngelsdorp, D., Tarpy, D.R., Lengerich, E.J., Pettis, J.S. (2013) Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. Prev. Vet. Med. 108(2–3), 225–233

    Article  PubMed  Google Scholar 

  • Waddington, K.D., Nelson, M., Page, R.E. (1998) Effects of pollen quality and genotype on the dance of foraging honey bees. Anim. Behav. 56, 35–39

    Article  PubMed  Google Scholar 

  • Wang, Y., Amdam, G.V., Rueppell, O., Wallrichs, M.A., Fondrk, M.K., Kaftanoglu, O., Page, R.E. (2009) PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 4(4), e4899

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang, Y., Kocher, S.D., Linksvayer, T.A., Grozinger, C.M., Page, R.E., Amdam, G.V. (2012) Regulation of behaviorally associated gene networks in worker honey bee ovaries. J. Exp. Biol. 215(1), 124–134

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang, Y., Mutti, N.S., Ihle, K.E., Siegel, A., Dolezal, A.G., Kaftanoglu, O., Amdam, G.V. (2010) Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet. 6(4), e1000896

    Article  PubMed Central  PubMed  Google Scholar 

  • Whitfield, C.W., Ben-Shahar, Y., Brillet, C., Leoncini, I., Crauser, D., Le Conte, Y., Rodriguez-Zas, S., Robinson, G.E. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc. Natl. Acad. Sci. U. S. A. 103(44), 16068–16075

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Williams, G.C. (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411

    Article  Google Scholar 

  • Zsolt Garamszegi, L., Marko, G., Herczeg, G. (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol. Ecol. 26(5), 1213–1235

    Article  Google Scholar 

Download references

Acknowledgements

I thank David Tarpy and Stan Schneider for the invitation to write this review. I am greatly indebted to Robert Page for introducing me to many fascinating problems that relate to pollen hoarding behavior in honey bees. I would also like to acknowledge the financial support of the National Institutes of Health grant (R15GM102753), the United States Department of Agriculture (2010-65104-20533), and the North American Pollinator Protection Campaign.

Author information

Authors and Affiliations

  1. Department of Biology, The University of North Carolina at Greensboro, 312 Eberhart Building, 321 McIver Street, Greensboro, NC, 27403, USA

    Olav Rueppell

Authors
  1. Olav Rueppell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olav Rueppell.

Additional information

Manuscript editor: David Tarpy

L’architecture génétique du syndrôme d’entassement du pollen chez les abeilles: incidences sur la compréhension de l’évolution sociale, des syndromes comportementaux et de l’élevage sélectif

Pleïotropie / syndrome comportemental / santé de l’abeille / évolution corrélée / sélection artificielle / ovaire

Struktur des Syndroms der Pollen-Vorratshaltung bei Honigbienen: Auswirkungen auf das Verständnis von sozialer Evolution, Verhaltenssyndromen und selektiver Zucht

Pleiotropie / Verhaltenssyndrome/Bienengesundheit / Sozialverhalten / korrelierte Evolution / künstliche selektion / Ovar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rueppell, O. The architecture of the pollen hoarding syndrome in honey bees: implications for understanding social evolution, behavioral syndromes, and selective breeding. Apidologie 45, 364–374 (2014). https://doi.org/10.1007/s13592-013-0244-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0244-3

Keywords

Search

Navigation