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Heritability of worker ovariole number in the Cape honey bee Apis mellifera capensis

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Abstract

In the honey bee (Apis mellifera), a key feature of the queen/worker caste dimorphism is a dramatic difference in ovariole number. However, even within the worker caste, variation in ovariole number is associated with the variance in reproductive potential. Workers of the Cape honey bee, A. m. capensis, are unique in that they are able to produce diploid female offspring asexually, and as a result, have a highly reproductive phenotype, a central feature of which is high ovariole number. We show that patrilines (subfamilies of full-sister workers sharing a father) within colonies vary significantly in ovariole number. Heritability of ovariole number was significantly greater than zero in two population samples (1991–1992: h 2 = 0.19 ± 0.11; 1992–1993: h 2 = 0.57 ± 0.19), suggesting a significant additive genetic as well as an environmental contribution to this trait. During the course of this study, we indirectly observed the replacement (supersedure) of a queen by her worker-produced granddaughter, providing confirmation of the reproductive potential of A. m. capensis workers.

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References

  • Aljanabi S.M. and Martinez I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids. Res. 25: 4692-4693

    Google Scholar 

  • Allsopp M.H., Beekman M., Gloag R.S. and Oldroyd B.P. 2010. Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis. Behav. Ecol. Sociobiol. 64: 567-574

    Google Scholar 

  • Allsopp M.H., Calis J.N.M. and Boot W.J. 2003. Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav. Ecol. Sociobiol. 54: 555-561

    Google Scholar 

  • Asencot M. and Lensky Y. 1976. The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. Life Sci. 18: 693-700

    Google Scholar 

  • Becker W.A. 1984. Manual of Quantitative Genetics. Academic enterprises, Pullman Washington

  • Beekman M., Allsopp M.H., Jordan L.A., Lim J. and Oldroyd B.P. 2009. A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis. Mol. Ecol. 18: 2722-2727

    Google Scholar 

  • Beekman M., Allsopp M.H., Lim J., Goudie F. and Oldroyd B.P. 2011. Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually. J. Hered. 102: 652-566

    Google Scholar 

  • Beekman M., Allsopp M.H., Wossler T.C. and Oldroyd B.P. 2008. Factors affecting the dynamics of the honeybee (Apis mellifera) hybrid zone of South Africa. Heredity 100: 13-18

    Google Scholar 

  • Beekman M., Calis J.N.M. and Boot W.J. 2000. Parasitic honeybees get royal treatment. Nature 404: 723

    Google Scholar 

  • Beekman M., Peeters C. and O’Rain M.J. 2006. Developmental divergence: neglected variable in understanding the evolution of reproductive skew in social animals. Behav. Ecol. 17: 622-627

    Google Scholar 

  • Calis J.N.M., Boot W.J., Allsopp M.H. and Beekman M. 2002. Getting more than a fair share: Nutrition of worker larvae related to social parasitism in the Cape honey bee Apis mellifera capensis. Apidologie 33: 193-202

    Google Scholar 

  • Dedej S., Hardfelder 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. Apic. Res. 37: 183-190

    Google Scholar 

  • Dzierzon J. 1845. Gutachten über die von Herrn Direktor Stöhr im ersten und zweiten Kapitel des General-Gutachtens aufgestellten Fragen. Eichstädter Bienenzeitung 1: 109-113, 119-121

    Google Scholar 

  • Estoup A., Solignac M. and Cornuet J-M. 1994. Precise assessment of the number of patrilines and of genetic relatedness in honey bee colonies. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 258: 1-7

    Google Scholar 

  • Evans J.D. and Wheeler D.E. 1999. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proc. Natl. Acad. Sci. USA 96: 5575-5580

  • Falconer D.S. and Mackay T.F.C. 1996. Introduction to Quantitative Genetics. Addison Wesley Longman, Harlow Essex

  • Goudie F., Allsopp H.M., Beekman M., Peter R.O., Lim J. and Oldroyd B.P. 2012. Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera capensis). Evolution doi: 10.1111/j.1558-5646.2011.01543.x

  • Greeff J.M. 1996a. Brief report: Thelytokous versus arrhenotokous worker reproduction in the Cape honeybee and other eusocial Hymenoptera. Hereditas (Lund) 124: 99-103

  • Greeff J.M. 1996b. Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 351: 617-625

  • Hartfelder K. and Engels W. 1998. Social insect polymorphism: Hormonal regulation of plasticity in development and reproduction in the honeybee. Curr. Top. Dev. Biol. 40: 45-77

    Google Scholar 

  • Hartfelder K., and Steinbruck G. 1997. Germ cell cluster formation and cell death are alternatives in caste-specific differentiation of the larval honey bee ovary. Invertebr. Reprod. Dev. 31: 237-250

    Google Scholar 

  • Hepburn H.R. and Crewe R.M. 1990. Defining the Cape honeybee: reproductive traits of queenless workers. S. Afr. J. Sci. 86: 524–527

    Google Scholar 

  • Hillesheim E., Koeniger N. and Moritz R.F.A. 1989. Colony performance in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate and dominant workers. Behav. Ecol. Sociobiol. 24: 291-296

    Google Scholar 

  • Holmes M.J., Oldroyd B.P., Allsopp M.H. and Beekman M. 2010. Maternity of emergency queens in the Cape honey bee, Apis mellifera capensis. Mol. Ecol. 19: 2792-2799

  • Jordan L.A., Allsopp M.H., Beekman M., Wossler T.C. and Oldroyd B.P. 2008a. Inheritance of traits associated with reproductive potential in Apis mellifera capensis and Apis mellifera scutellata workers. J. Hered. 99: 376-381

  • Jordan L.A., Allsopp M.H., Oldroyd B.P., Wossler T.C. and Beekman M. 2008b. Cheating honeybee workers produce royal offspring. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 275: 345-351

  • Lattorff H.M.G., Moritz R.F.A., Crewe R.M. and Solignac M. 2007. Control of reproductive dominance by the thelytoky gene in honeybees. Biol. Lett. 3: 292-295

    Google Scholar 

  • Linksvayer T.A., Rueppell O., Siegel A., Kaftanoglu O., Page R.E. and Amdam G.V. 2009. The genetic basis of transgressive ovary size in honeybee workers. Genetics 183: 693-707

    Google Scholar 

  • Lyko F., Forst S., Kucharski R., Wolf S., Falckenhayn C. and Maleszka R. 2010. The honey bee epigenomerential methylation of brain DNA in queens and workers. PLoS Biol. 8: e1000506

    Google Scholar 

  • Makert G.R., Paxton R.J. and Hartfelder K. 2006. Ovariole number - a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav. Ecol. Sociobiol. 60: 815-825

    Google Scholar 

  • Michener C.D. 1974. The Social Behavior of the Bees. Harvard University Press, Cambridge Massachusetts

  • Michener C.D. 2000. The Bees of the World. John Hopkins University Press, Baltimore London

  • Montague C.E. and Oldroyd B.P. 1998. The evolution of worker sterility in honey bees: an investigation into a behavioral mutant causing a failure of worker policing. Evolution 52: 1408-1415

    Google Scholar 

  • Moritz R.F.A. and Hillesheim E. 1985. Inheritance of dominance in honeybees Apis mellifera capensis. Behav. Ecol. Sociobiol. 17: 87-89

    Google Scholar 

  • Moritz R.F.A., Kryger P. and Allsopp M.H. 1996. Competition for royalty in bees. Nature 384: 31

    Google Scholar 

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

    Google Scholar 

  • Oldroyd B.P. and Moran C. 1983. Heritability of worker characters in the honeybee (Apis mellifera). Aust. J. Biol. Sci. 36: 323-332

    Google Scholar 

  • Oldroyd B.P., Rinderer T.E. and Buco S. 1991. Heritability of morphological characters used to distinguish European and Africanized honey bees. Theor. Appl. Genet. 82: 499-504

    Google Scholar 

  • Oldroyd B.P., Wossler T.C. and Ratnieks F.L.W. 2001. Regulation of ovary activation in worker honey-bees (Apis mellifera): larval signal production and adult response thresholds differ between anarchistic and wild-type bees. Behav. Ecol. Sociobiol. 50: 366-377

    Google Scholar 

  • Onions G.W. 1912. South African ‘fertile worker bees’. Agric. J. Union of S. Afr. 1: 720-728

    Google Scholar 

  • Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236

    Google Scholar 

  • Roff D.A. 1997. Evolutionary Quantitative Genetics. Chapman and Hall, New York

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

    Google Scholar 

  • Ruttner F. 1977. The problem of cape bee (Apis mellifera capensis Escholtz) - Parthenogenesis - Size of population - Evolution. Apidologie 8: 281-294

    Google Scholar 

  • Schmidt Capella I.C. and Hartfelder K. 1998. Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. J. Insect Physiol. 44: 385-391

    Google Scholar 

  • Schmidt Capella I.C. and Hartfelder K. 2002. Juvenile hormonedependent interaction of actin and spectrin in polymorphic differentiation of the larval honey bee ovary. Cell Tissue Res. 307: 265-272

    Google Scholar 

  • Shaibi T., Lattorff H.M.G. and Moritz R.F.A. 2008. A microsatellite DNA toolkit for studying population structure in Apis mellifera. Mol. Ecol. Res. 8: 1034-1036

    Google Scholar 

  • Shuel R.W. and Dixon S.E. 1959. Studies in the mode of action of royal jelly in honeybee development. II. Respiration of newly emerged larvae on various substrates. Can. J. Zool. 37: 803-813

    Google Scholar 

  • Starr C.K. 1979. Origin and evolution of insect sociality. In: Social Insects, Vol. I (Hermann H.R., Ed), Academic Press, London. pp 35-79

  • Vergoz V., Lim J. and Oldroyd B.P. 2012. Biogenic amine receptor gene expression in the ovarian tissue of the honey bee Apis mellifera. Insect. Mol. Biol. (in press)

  • Verma S. and Ruttner F. 1983. Cytological analysis of thelytokous parthenogenesis in the Cape honey bee Apis mellifera capensis. Apidologie 14: 41-57

    Google Scholar 

  • White M.J.D. 1973. Animal Cytology and Evolution, 3 Edn. Cambridge University Press, Cambridge

  • Wilson E.O. 1975. Sociobiology. The New Synthesis. Harvard University Press, Cambridge

  • Wilson E.O. and Hölldobler B. 2005. Eusociality: Origin and consequences. Proc. Natl. Acad. Sci. USA 102: 13367-13371

    Google Scholar 

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

  • Wirtz P. and Beetsma J. 1972. Induction of caste differentiation in the honey bee (Apis mellifera) by juvenile hormone. Entomol. Exp. Appl. 15: 517-520

    Google Scholar 

  • Woyke J. 1999. Increased food supply to all larvae after dequeening honey bee colonies. J. Apic. Res. 38: 117-123

    Google Scholar 

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Acknowledgments

The work was supported by Australian Research Council grants to M. Beekman and B. Oldroyd.

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Correspondence to F. Goudie.

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Goudie, F., Allsopp, M.H., Beekman, M. et al. Heritability of worker ovariole number in the Cape honey bee Apis mellifera capensis . Insect. Soc. 59, 351–359 (2012). https://doi.org/10.1007/s00040-012-0227-9

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