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Experimentally induced variation in the physical reproductive potential and mating success in honey bee queens

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Abstract

In honeybee colonies, reproduction is monopolized by the queen while her daughter workers are facultatively sterile. Caste determination is a consequence of environmental conditions during development, during which female larvae may become either queens or workers depending on their larval diet. This bipotency introduces significant variation in the reproductive potential of queen bees, with queens raised from young worker larvae exhibiting high reproductive potential and queens raised from older worker larvae exhibiting lower reproductive potential. We verify that low-quality queens are indeed produced from older worker larvae, as measured morphometrically (e.g., body size) and by stored sperm counts. We also show, for the first time, that low-quality queens mate with significantly fewer males, which significantly influences the resultant intracolony genetic diversity of the worker force of their future colonies. These results demonstrate a reproductive continuum of honeybee queens and provide insights into the reproductive constraints of social insects.

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References

  • Barchuk A.R., Cristino A.S., Kucharski R., Costa L.F., Simoes Z.L.P. and Maleszka R. 2007. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Devel. Biol. 7: 70

    Google Scholar 

  • Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. B 351: 947-975

    Google Scholar 

  • Cobey S. 2003. The extraordinary honey bee mating strategy and a simple field dissection of the spermatheca—A three-part series—Part 3—The spermatheca. Am. Bee J. 143: 217-220

    Google Scholar 

  • Collins A.M. and Donoghue A.M. 1999. Viability assessment of honey bee, Apis mellifera sperm using dual fluorescent staining. Theriogenology 51: 1513-1523

    Google Scholar 

  • Crozier R.H. and Pamilo P. 1996. Evolution of Social Insect Colonies: Sex Allocation and Kin Selection. Oxford University Press, New York. 306 pp

  • de Azevedo S.V. and Hartfelder K. 2008. The insulin signaling pathway in honey bee (Apis mellifera) caste development - differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J. Insect Physiol. 54: 1064-1071

    Google Scholar 

  • Dedej S., Hartfelder K., Aumeier P., Rosenkranz P. and Engels W. 1998. Caste determination is a sequential process: effect of larval age at grafting on ovariole number, hind leg size and cephalic volatiles in the honey bee (Apis mellifera carnica). J. Apicult. Res. 37: 183-190

    Google Scholar 

  • Delaney D.A., Keller J.J., Caren J.R. and Tarpy D.R. 2011. The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera). Apidologie 42: 1-13

    Google Scholar 

  • Eckert J.E. 1934. Studies in the number of ovarioles in queen honeybees in relation to body size. J. Econ. Entomol. 27: 629-635

    Google Scholar 

  • Fjerdingstad E.J. and Keller L. 2004. Relationships between phenotype, mating behavior, and fitness of queens in the ant Lasius niger. Evolution 58: 1056-1063

    Google Scholar 

  • Franck P., Coussy H., Le C.Y., Solignac M., Garnery L. and Cornuet J.M. 1999. Microsatellite analysis of sperm admixture in honeybee. Insect Mol. Biol. 8: 419-421

    Google Scholar 

  • Franck P., Solignac M., Vautrin D., Cornuet J.M., Koeniger G. and Koeniger N. 2002. Sperm competition and last-male precedence in the honeybee. Anim. Behav. 64: 503-509

    Google Scholar 

  • Gary N.E. 1963. Observations of mating behaviour in the honeybee. J. Apicult. Res. 2: 3-13

    Google Scholar 

  • Gilley D.C., Tarpy D.R. and Land B.B. 2003. The effect of queen quality on the interactions of workers and dueling queen honey bees (Apis mellifera L.). Behav. Ecol. Sociobiol. 55: 190-196

    Google Scholar 

  • Haberl M. and Tautz D.1998. Sperm usage in honey bees. Behav. Ecol. Sociobiol. 423: 247-255

    Google Scholar 

  • Hatch S., Tarpy D.R. and Fletcher D.J.C. 1999. Worker regulation of emergency queen rearing in honey bee colonies and the resultant variation in queen quality. Insect. Soc. 46: 372-377

    Google Scholar 

  • Hayworth M.K., Johnson N.G., Wilhelm M.E., Gove R.P., Metheny J.D. and Rueppell O. 2009. Added weights lead to reduced flight behavior and mating success in polyandrous honey bee queens (Apis mellifera). Ethology 115: 698-706

    Google Scholar 

  • Kocher S.D., Richard F.J., Tarpy D.R. and Grozinger C.M. 2008. Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9: 232

    Google Scholar 

  • Koeniger G. 1988. Mating behavior of honey bees. In: Africanized Honey Bees and Bee Mites (Brown C.E., Ed), Wiley and Sons, New York. pp 167-172

  • Laidlaw H.H. Jr. and Page R.E. Jr. 1984. Polyandry in honey bees (Apis mellifera L.): sperm utilization and intracolony genetic relationships. Genetics 108: 985-997

    Google Scholar 

  • Laidlaw H.H. Jr. and Page R.E. Jr. (1997). Queen Rearing and Bee Breeding. Wicwas, Cheshire, CT. 224 pp

  • Mattila H.R. and Seeley T.D. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364

    Google Scholar 

  • Nelson D.L. and Gary N.E. 1983. Honey productivity of honey bee Apis mellifera colonies in relation to body weight attractiveness and fecundity of the queen. J. Apicult. Res. 22: 209-213

    Google Scholar 

  • Nielsen R., Tarpy D.R. and Reeve H.K. 2003. Estimating effective paternity number in social insects and the effective number of alleles in a population. Molec. Ecol. 12: 3157-3164

    Google Scholar 

  • Oldroyd B.P. and Fewell J.H. 2007. Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22: 408-413

    Google Scholar 

  • Page R.E. Jr. 1980 The evolution of multiple mating behavior by honey bee queens (Apis mellifera). Genetics 96: 263-273

    Google Scholar 

  • Page R.E. Jr., Kimsey R.B. and Laidlaw H.H. Jr. 1984. Migration and dispersal of spermatozoa in spermathecae of queen honeybees (Apis mellifera L.). Experientia 40: 182-184

    Google Scholar 

  • Page R.E. Jr., Robinson G.E., Fondrk M.K. and Nasr M.E. 1995. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav. Ecol. Sociobiol. 36: 387-396

    Google Scholar 

  • Ratnieks F.L.W. 1990. The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males. Behav. Ecol. Sociobiol. 26: 343-348

    Google Scholar 

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

    Google Scholar 

  • Ruttner F. 1956. The mating of the honeybee. Bee World 37: 3-15

    Google Scholar 

  • Sasaki K., Satoh T. and Obara Y. 1995. Sperm utilization by honey bee queens; DNA fingerprinting analysis. Appl. Entomol. Zool. 30: 335-341

    Google Scholar 

  • Schluns H., Moritz R.F.A., Neumann P., Kryger P. and Koeniger G. 2005. Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. Anim. Behav. 70: 125-131

    Google Scholar 

  • Seeley T.D. and Tarpy D.R. 2007. Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. B 274: 67-72

    Google Scholar 

  • Tanaka E.D. and Hartfelder K. 2004. The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct. Dev. 33: 431-442

    Google Scholar 

  • Tarapore D., Floreano D. and Keller L. 2010. Task-dependent influence of genetic architecture and mating frequency on division of labour in social insect societies. Behav. Ecol. Sociobiol. 64: 675-684

    Google Scholar 

  • Tarpy D.R. 2003. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. Lond. B 270: 99-103

    Google Scholar 

  • Tarpy D.R., Caren J.R., Delaney D.A., Sammataro D., Finley J., Loper G.M. and DeGrandi-Hoffman G. 2010. Mating frequencies of Africanized honey bees in the south western USA. J. Apicult. Res. 49: 302-310

    Google Scholar 

  • Tarpy D.R. and Mayer M.K. 2009. The effects of size and reproductive quality on the outcomes of duels between honey bee queens (Apis mellifera L.). Ethol. Ecol. Evol. 21: 147-153

    Google Scholar 

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

    Google Scholar 

  • Tarpy D.R., Nielsen R. and Nielsen D.I. 2004. A scientific note on the revised estimates of effective paternity frequency in Apis. Insect. Soc. 51: 203-204

    Google Scholar 

  • Tarpy D.R. and Page R.E. Jr. 2000. No behavioral control over mating frequency in queen honey bees (Apis mellifera L.): Implications for the evolution of extreme polyandry. Am. Nat. 155: 820-827

    Google Scholar 

  • Tarpy D.R. and Page R.E. Jr. 2001. The curious promiscuity of queen honey bees (Apis mellifera): evolutionary and behavioral mechanisms. Ann. Zool. Fenn. 38: 255-265

    Google Scholar 

  • Toth A.L., Bilof K.B.J., Henshaw M.T., Hunt J.H. and Robinson G.E. 2009. Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insect. Soc. 56: 77-84

  • Ugelvig L.V., Kronauer D.J.C., Schrempf A., Heinze J. and Cremer S. 2010. Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc. R. Soc. B 277: 2821-2828

    Google Scholar 

  • Waddington S.J., Santorelli L.A., Ryan F.R. and Hughes W.O.H. 2010. Genetic polyethism in leaf-cutting ants. Behav. Ecol. 21: 1165-1169

    Google Scholar 

  • Walker W.F. 1980. Sperm utilization strategies in nonsocial insects. Am. Nat. 115: 780-799

    Google Scholar 

  • Wang J.L. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963–1979.

    Google Scholar 

  • Wilson E.O. 1971. The Insect Societies. Harvard University Press, Cambridge. 548 pp

  • Winston M.L. 1987. The Biology of the Honey Bee. Harvard University Press, Cambridge. 281 pp

  • Withers G.S., Fahrbach S.E. and Robinson G.E. 1995. Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J. Neurobiol. 26: 130-144

    Google Scholar 

  • Woyke J. 1964. Causes of repeated mating flights by queen honeybees. J. Apicult. Res. 3: 17-23

    Google Scholar 

  • Woyke J. 1971. Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens, and results of insemination. J. Apicult. Res. 10: 45-55

    Google Scholar 

  • Woyke J. 1989. Results of instrumental insemination. In: The Instrumental Insemination of the Queen Bee (Moritz R.F.A., Ed), Apimondia, Bucharest. pp 93-103

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Acknowledgments

We thank Jessica Richards, Matt Mayer, and Holly Wantuch for their help in collecting data in the field, as well as John Harman for his help in DNA extractions and PCR analyses. A special thanks goes to Laura Mathies for use of her fluorescent microscope for the sperm analyses, as well as Laurent Keller and Jim Hunt for helpful comments on the manuscript. Consuelo Arellano provided helpful statistical advice that improved the manuscript. This study was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2007-02281.

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Authors and Affiliations

  1. Department of Entomology, North Carolina State University, Campus Box 7613, Raleigh, NC, USA

    D. R. Tarpy, J. J. Keller & J. R. Caren

  2. Keck Center for Behavioral Biology, North Carolina State University, Campus Box 7613, Raleigh, NC, USA

    D. R. Tarpy

  3. Department of Entomology and Wildlife Biology, University of Delaware, 252 Townsend Hall, Newark, DE, 19716, USA

    D. A. Delaney

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  1. D. R. Tarpy
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Correspondence to D. R. Tarpy.

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Tarpy, D.R., Keller, J.J., Caren, J.R. et al. Experimentally induced variation in the physical reproductive potential and mating success in honey bee queens. Insect. Soc. 58, 569–574 (2011). https://doi.org/10.1007/s00040-011-0180-z

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