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Insectes Sociaux

, Volume 65, Issue 4, pp 601–608 | Cite as

Do queen cuticular hydrocarbons inhibit worker reproduction in Bombus impatiens?

  • V. Melgarejo
  • E. E. Wilson Rankin
  • K. J. Loope
Research Article

Abstract

Social insect colonies are organized by a reproductive division of labor, in which non-reproductive workers cooperate to rear the offspring of the queen. Queen pheromones, chemical compounds produced by queens that regulate worker fertility, have been identified in a handful of bees, ants, wasps, and termites. However, recent studies on bumblebee (Bombus spp.) queen signals have yielded conflicting findings. Here we provide an independent investigation of experiments to test the hypothesis that queen-produced non-volatile cuticular compounds influence worker’s reproductive behavior. We exposed small groups of Bombus impatiens workers to extracted cuticular compounds from queens collected from either mid-season (pre-reproductive) or late-season (reproductive) colonies and tracked worker reproduction and ovary development. We observed no difference in worker’s ovarian development or egg production when comparing among the mid-season queen extract, late-season queen extract and the solvent control treatments. Our data replicate the finding that body size positively correlates with ovarian development in workers. These results are consistent with recent studies showing that queen cuticular compounds do not inhibit worker reproduction in B. impatiens.

Keywords

Queen pheromone Worker reproduction Cuticular hydrocarbons 

Notes

Acknowledgements

We thank Biobest for providing bumblebee colonies, and Hollis Woodard for providing the frozen late-season queens used in Experiment I. Etya Amsalem, Jenny Jandt and Jocelyn Millar provided helpful advice. Funding for this project came from fellowships to V. M. from UCR Research in Science and Engineering (RISE) summer program and California Alliance for Minority Participation (CAMP-UCR). K. J. L. was supported by a USDA-NIFA postdoctoral fellowship.

References

  1. Amsalem E, Twele R, Francke W, Hefetz A (2009) Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc R Soc Lond Ser B Biol Sci 276:1295CrossRefGoogle Scholar
  2. Amsalem E, Kiefer J, Schulz S, Hefetz A (2014) The effect of caste and reproductive state on the chemistry of the cephalic labial glands secretion of Bombus terrestris. J Chem Ecol 40:900–912CrossRefGoogle Scholar
  3. Amsalem E, Grozinger CM, Padilla M, Hefetz A (2015a) The physiological and genomic bases of bumble bee social behaviour. Adv Insect Phys 48:37–93CrossRefGoogle Scholar
  4. Amsalem E, Orlova M, Grozinger CM (2015b) A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens). Proc R Soc Lond Ser B Biol Sci 282:20151800CrossRefGoogle Scholar
  5. Amsalem E, Padilla M, Schreiber PM et al (2017) Do bumble bee, Bombus impatiens, queens signal their reproductive and mating status to their workers? J Chem Ecol 43:563–572.  https://doi.org/10.1007/s10886-017-0858-4 CrossRefPubMedGoogle Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  7. Bloch G, Hefetz A (1999) Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies. J Chem Ecol 25:881–896CrossRefGoogle Scholar
  8. Bourke AFG (1994) Worker matricide in social bees and wasps. J Theor Biol 167:283–292CrossRefGoogle Scholar
  9. Bourke AFG, Ratnieks FLW (2001) Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae). Proc R Soc Lond Ser B Biol Sci 268:347–355CrossRefGoogle Scholar
  10. Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linn Soc 91:161–188.  https://doi.org/10.1111/j.1095-8312.2007.00784.x CrossRefGoogle Scholar
  11. Cnaani J, Schmid-Hempel R, Schmidt JO (2002) Colony development, larval development and worker reproduction in Bombus impatiens Cresson. Insectes Soc 49:164–170CrossRefGoogle Scholar
  12. Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107:186–207CrossRefGoogle Scholar
  13. Gradish AE, Scott-Dupree CD, Mcfarlane AD, Frewin AJ (2013) Too much work, not enough tarsi: group size influences Bombus impatiens (Hymenoptera: Apidae) worker reproduction with implications for sublethal pesticide toxicity assessments. J Econ Entomol 106:552–557.  https://doi.org/10.1603/EC12154 CrossRefPubMedGoogle Scholar
  14. Holman L (2014) Bumblebee size polymorphism and worker response to queen pheromone. PeerJ 2:e604CrossRefGoogle Scholar
  15. Holman L, Jørgensen CG, Nielsen J, d’Ettorre P (2010) Identification of an ant queen pheromone regulating worker sterility. Proc R Soc Lond Ser B Biol Sci 277:3793CrossRefGoogle Scholar
  16. Holman L, Lanfear R, d’Ettorre P (2013) The evolution of queen pheromones in the ant genus Lasius. J Evol Biol 26:1549–1558CrossRefGoogle Scholar
  17. Holman L, Hanley B, Millar JG (2016) Highly specific responses to queen pheromone in three Lasius ant species. Behav Ecol Sociobiol 70:387–392.  https://doi.org/10.1007/s00265-016-2058-6 CrossRefGoogle Scholar
  18. Holman L, van Zweden JS, Oliveira RC et al (2017) Conserved queen pheromones in bumblebees: a reply to Amsalem et al. PeerJ 5:e3332.  https://doi.org/10.7717/peerj.3332 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480.  https://doi.org/10.1007/s00114-003-0462-z CrossRefGoogle Scholar
  20. Jandt JM, Dornhaus A (2011) Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life. Behav Ecol Sociobiol 65:2341–2349CrossRefGoogle Scholar
  21. Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794CrossRefGoogle Scholar
  22. Kelly CD (2006) Replicating empirical research in behavioral ecology: how and why it should be done but rarely ever is. Q Rev Biol 81:221–236.  https://doi.org/10.1086/506236 CrossRefPubMedGoogle Scholar
  23. Lin H, Winston ML (1998) The role of nutrition and temperature in the ovarian development of the worker honey bee (Apis mellifera). Can Entomol 130:883–891.  https://doi.org/10.4039/Ent130883-6 CrossRefGoogle Scholar
  24. Matsuura K, Himuro C, Yokoi T et al (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci 107:12963–12968.  https://doi.org/10.1073/pnas.1004675107 CrossRefPubMedGoogle Scholar
  25. Oi CA, Van Zweden JS, Oliveira RC et al (2015) The origin and evolution of social insect queen pheromones: novel hypotheses and outstanding problems. BioEssays 37:808–821CrossRefGoogle Scholar
  26. Oi CA, Millar JG, Van Zweden JS, Wenseleers T (2016) Conservation of queen pheromones across two species of vespine wasps. J Chem Ecol 42:1175–1180CrossRefGoogle Scholar
  27. Padilla M, Amsalem E, Altman N et al (2016) Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens. R Soc Open Sci 3:160576CrossRefGoogle Scholar
  28. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 1 Mar 2018
  29. Rottler-Hoermann A-M, Schulz S, Ayasse M (2016) Nest wax triggers worker reproduction in the bumblebee Bombus terrestris. R Soc Open Sci 3:150599CrossRefGoogle Scholar
  30. Röseler PF, Röseler I, van Honk CGJ (1981) Evidence for inhibition of corpora allata activity in workers of Bombus terrestris by a pheromone from the queen’s mandibular glands. Experientia 37:348–351.  https://doi.org/10.1007/BF01959856 CrossRefGoogle Scholar
  31. Smith AA, Liebig J (2017) The evolution of cuticular fertility signals in eusocial insects. Curr Opin Insect Sci 22:79–84CrossRefGoogle Scholar
  32. Smith AA, Holldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81CrossRefGoogle Scholar
  33. Smith AA, Millar JG, Suarez AV (2015) A social insect fertility signal is dependent on chemical context. Biol Lett 11:20140947CrossRefGoogle Scholar
  34. Therneau T (2015) A package for survival analysis in S. version 2.38. https://CRAN.R-project.org/package=survival
  35. Van Oystaeyen A, Oliveira RC, Holman L et al (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290.  https://doi.org/10.1126/science.1244899 CrossRefGoogle Scholar
  36. Wilson EO (1971) The insect societies. Belknap Press, CambridgeGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of California, RiversideRiversideUSA

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