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Geographic variation in polyandry of the Eastern Honey Bee, Apis cerana, in Thailand

Abstract

The repeated evolution of extreme polyandry in advanced social insects is exceptional and its explanation has attracted significant attention. However, most reported estimates of the number of matings are derived from limited sampling. Temporal and geographic variation in mating behavior of social insects has not been sufficiently studied. Worker offspring of 18 Eastern Honey Bee (Apis cerana Fabr.) queens from three populations across Thailand were genotyped at five microsatellite markers to test for population differences of mating behavior across three different ecosystems. The number of matings decreased from a northern, more seasonal environment to a southern tropical population and was lowest in a tropical island population. Our study confirms earlier findings that social insect mating behavior shows biogeographic variation and highlights that data from several populations are needed for reliable species-specific estimates of the number of matings. Populations that show significant differentiation in the number of matings may be studied to discriminate effectively among the different hypotheses that have been proposed to explain the evolution of polyandry in honey bees and other advanced social insects.

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References

  • Brown M.J.F. and Schmid-Hempel P. 2003. The evolution of female multiple mating in social Hymenoptera. Evolution 57: 2067–2081

  • Cole B.J. 1983. Multiple mating and the evolution of social behavior in the Hymenoptera. Behav. Ecol. Sociobiol. 12: 191–201

  • Corley M. and Fjerdingstad E.J. 2011. Mating strategies of queens in Lasius niger ants-is environment type important? Behav. Ecol. Sociobiol. 65: 889–897

  • Crozier R.H. and Fjerdingstad E.J. 2001. Polyandry in social Hymenoptera—disunity in diversity? Ann. Zool. Fenn. 38: 267–285

  • Crozier R.H. and Page R.E. 1985. On being the right size—male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol. 18: 105–115

  • El-Niweiri M.A.A. and Moritz R.F.A. 2011. Mating in the rain? Climatic variance for polyandry in the honeybee (Apis mellifera jemenitica) Popul. Ecol. 53: 421–427

  • Fjerdingstad E.J. and Boomsma J.J. 2000. Queen mating frequency and relatedness in young Atta sexdens colonies. Insect. Soc. 47: 354–356

  • Foster S.A. 1999. The geography of behaviour: an evolutionary perspective. Trends Ecol. Evol. 14: 190–195

  • Franck P., Koeniger N., Lahner G., Crewe R.M. and Solignac M. 2000. Evolution of extreme polyandry: an estimate of mating frequency in two African honeybee subspecies, Apis mellifera monticola and A.m. scutellata. Insect. Soc. 47: 364–370

  • Goodisman M.A.D., Matthews R.W. and Crozier R.H. 2002. Mating and reproduction in the wasp Vespula germanica. Behav. Ecol. Sociobiol. 51: 497–502

  • 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

  • Hughes W.O., Oldroyd B.P., Beekman M., Ratnieks F.L.W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213–1216

  • Jones O.R. and Wang J. 2010. COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol. Ecol. Res. 10: 551–555

  • Kraus F.B., Neumann P., van Praagh J. and Moritz R.F.A. 2004. Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav. Ecol. Sociobiol. 55: 494–501

  • Kronauer D.J.C., Johnson R.A. and Boomsma J.J. 2007. The evolution of multiple mating in army ants. Evolution 61: 413–422

  • Mattila H.R., Reeve H.K. and Smith M.L. 2012. Promiscuous honey bee queens increase colony productivity by suppressing worker selfishness. Curr. Biol. 22: 2027–2031

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

  • 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. Mol. Ecol. 12: 3157–3164

  • Oldroyd B.P., Clifton M.J., Parker K., Wongsiri S., Rinderer T.E. and Crozier R.H. 1998. Evolution of mating behavior in the genus Apis and an estimate of mating frequency in Apis cerana (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 91: 700–709

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

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

  • Rattanawannee A., Chanchao C., Wongsiri S. and Oldroyd B.P. 2012. No evidence that habitat disturbance affects mating frequency in the giant honey bee Apis dorsata. Apidologie 43: 761–770

  • Rozalski R.J., Sakurai H., Tsuchida K. and Inoue A. 1996. Esterase and malate dehydrogenase isozymes analysis in the population of honeybee, Apis cerana japonica and Apis mellifera. Jap. J. Entomol. 64: 910–917

  • Rueppell O., Hayes A.M., Warrit N. and Smith D.R. 2011. Population structure of Apis cerana in Thailand reflects biogeography and current gene flow rather than Varroa mite association. Insect. Soc. 58: 445–452

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

  • Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Springer, Berlin.

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

  • Sherman P.W., Seeley T.D. and Reeve H.K. 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131: 602–610

  • Solignac M., Mougel F., Vautrin D., Monnerot M. and Cornuet J.M. 2007. A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol. 8: R66

  • Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1–13

  • Takahashi J.I., Shimizu S., Koyama S., Kimura K., Shimizu I. and Yoshida T. 2009. Variable microsatellite loci isolated from the Asian honeybee, Apis cerana (Hymenoptera; Apidae). Mol. Ecol. Res. 9: 819–821

  • 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. Amer. 95: 513–528

  • 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

  • Warrit N., Smith D.R. and Lekprayoon C. 2006. Genetic subpopulations of Varroa mites and their Apis cerana hosts in Thailand. Apidologie 37: 19–30

  • Wattanachaiyingcharoen W., Oldroyd B.P., Wongsiri S., Palmer K. and Paar R. 2003. A scientific note on the mating frequency of Apis dorsata. Apidologie 34: 85–86

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Acknowledgments

This work was supported by UNCG, Chiang Mai University, the US National Institute of Food and Agriculture (AFRI Grant: #2010-65104-20533), the US National Science Foundation (Grant: #0926288), and the National Institutes of Health (NIGMS, Grant: #R15GM102753). We would like to thank Werapon Honjam, Bobbee Vannasane, the UNCG Social Insect Lab, and Panuwan Chantawannakul for their helpful advice, kind hospitality, and practical help in collecting the samples and extracting DNA.

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Correspondence to O. Rueppell.

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DeFelice, D.S., Ross, C., Simone-Finstrom, M. et al. Geographic variation in polyandry of the Eastern Honey Bee, Apis cerana, in Thailand. Insect. Soc. 62, 37–42 (2015). https://doi.org/10.1007/s00040-014-0371-5

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  • DOI: https://doi.org/10.1007/s00040-014-0371-5

Keywords

  • Polyandry
  • Social evolution
  • Behavioral ecology
  • Division of labor
  • Honeybees
  • Apis cerana
  • Biogeographic variation