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Behavioral Ecology and Sociobiology

, Volume 69, Issue 9, pp 1511–1518 | Cite as

Reproductive physiology mediates honey bee (Apis mellifera) worker responses to social cues

  • David A. GalbraithEmail author
  • Ying Wang
  • Gro V. Amdam
  • Robert E. Page
  • Christina M. Grozinger
Original Paper

Abstract

Though social insect colonies are often considered to be models of cooperative behavior, there can be conflict between queens and their workers over reproduction. In honey bees (Apis mellifera), the queen releases a pheromone that attracts workers and inhibits worker ovary activation such that they remain sterile and rear the offspring of the queen. Furthermore, under queenless conditions, workers can rear new queens from the old queen’s eggs or activate their ovaries and lay their own eggs. Workers vary greatly in their ability to activate their ovaries, and this variation is positively correlated with ovary size. Here, we demonstrate that, compared to their sisters, workers with the larger ovaries are less attracted to queen pheromone, less likely to rear new queens if the old queen is lost, and more likely to activate their ovaries in the absence of a queen. Furthermore, surgically increasing a bee’s ovarian mass reduces her attraction to queen pheromone. The additional ovarian mass altered brain expression levels of the octopamine receptor, Oa1, but these differences did not correlate with response to queen pheromone. Overall, these results indicate that honey bee workers’ response to social cues under both queenright and queenless contexts is modified by their reproductive physiology, such that workers with greater ovary activation rates are less likely to engage in behaviors that promote the queen’s reproduction.

Keywords

Honey bee Conflict Altruism Reproduction Pheromone 

Notes

Acknowledgments

We want to thank Dr. Osman Kaftanoglu, Bernardo Niño, and Dr. Elina Lastro Niño for preparing the bee colonies. We would also like to thank Dr. Adam Dolezal for help with ovary dissections.

Conflict of interest

The authors have no competing interests.

Supplementary material

265_2015_1963_MOESM1_ESM.xlsx (10 kb)
ESM 1 (XLSX 9 kb)

References

  1. Allsopp MH, Calis JNM, Boot WJ (2003) Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav Ecol Sociobiol 54:555–561. doi: 10.1007/s00265-003-0666-4 CrossRefGoogle Scholar
  2. Amdam GV, Csondes A, Fondrk MK, Page RE (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439:76–78. doi: 10.1038/nature04340 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Amdam GV, Page RE, Fondrk MK, Brent CS (2010) Hormone response to bidirectional selection on social behavior. Evol Dev 12:428–436. doi: 10.1111/j.1525-142X.2010.00429.x PubMedCentralCrossRefPubMedGoogle Scholar
  4. Barron AB, Oldroyd BP, Ratnieks FLW (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: areview. Behav Ecol Sociobiol 50:199–208. doi: 10.1007/s002650100362 CrossRefGoogle Scholar
  5. Calis JNM, Boot WJ, Allsopp MH, Beekman M (2006) Getting more than a fair share: nutrition of worker larvae related to social parasitism in the Cape honey bee Apis mellifera capensis. Apidologie 37:452–461. doi: 10.1051/apido CrossRefGoogle Scholar
  6. Erber J, Kloppenburg P, Scheidler A (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073–1083. doi: 10.1007/BF01929916 CrossRefGoogle Scholar
  7. Fussnecker BL, McKenzie AM, Grozinger CM (2013) cGMP modulates responses to queen mandibular pheromone in worker honey bees. J Comp Physiol A Sensory Neural Behav Physiol 197:939–948. doi: 10.1007/s00359-011-0654-5.cGMP CrossRefGoogle Scholar
  8. Graham AM, Munday MD, Kaftanoglu O et al (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. doi: 10.1186/1471-2148-11-95 PubMedCentralCrossRefPubMedGoogle Scholar
  9. Grozinger CM, Robinson GE (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 193:461–470. doi: 10.1007/s00359-006-0202-x CrossRefGoogle Scholar
  10. Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–16CrossRefPubMedGoogle Scholar
  11. Hartfelder K, Bitondi MMG, Santana WC, Simões ZLP (2002) Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect Biochem Mol Biol 32:211–216. doi: 10.1016/S0965-1748(01)00100-X CrossRefPubMedGoogle Scholar
  12. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480. doi: 10.1007/s00114-003-0462-z CrossRefPubMedGoogle Scholar
  13. Hoover SER, Higo HA, Winston ML (2006) Worker honey bee ovary development: seasonal variation and the influence of larval and adult nutrition. J Comp Physiol B Biochem Syst Environ Physiol 176:55–63. doi: 10.1007/s00360-005-0032-0 CrossRefGoogle Scholar
  14. Kamakura M (2011) Royalactin induces queen differentiation in honeybees. Nature 473:478–483. doi: 10.1038/nature10093 CrossRefPubMedGoogle Scholar
  15. Katzav-Gozansky T, Boulay R, Soroker V, Hefetz A (2004) Queen-signal modulation of worker pheromonal composition in honeybees. Proc Biol Sci 271:2065–2069. doi: 10.1098/rspb.2004.2839 PubMedCentralCrossRefPubMedGoogle Scholar
  16. Kocher SD, Grozinger CM (2011) Cooperation, conflict, and the evolution of queen pheromones. J Chem Ecol 37:1263–1275. doi: 10.1007/s10886-011-0036-z CrossRefPubMedGoogle Scholar
  17. Kocher SD, Ayroles JF, Stone EA, Grozinger CM (2010) Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. PLoS One 5, e9116. doi: 10.1371/journal.pone.0009116 PubMedCentralCrossRefPubMedGoogle Scholar
  18. Laidlaw HH, Page RE (1997) Queen rearing and bee breeding, 1st edn. Wicwas Press, Cheshire, ConnecticutGoogle Scholar
  19. Le Conte YL, Sreng L, Sacher N et al (1994) Chemical recognition of queen cells by honey bee workers Apis mellifera (Hymenoptera: Apidae). Chemoecology 5–6:6–12. doi: 10.1007/BF01259967 CrossRefGoogle Scholar
  20. Le Conte Y, Sreng L, Poitout SH (1995) Brood pheromone con modulate the feeding behavior of Apis Mellifera workers (Hymenoptera: Apidea). J Econ Entomol 8:798–804CrossRefGoogle Scholar
  21. Makert GR, Paxton RJ, 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. doi: 10.1007/s00265-006-0225-x CrossRefGoogle Scholar
  22. Malka O, Shnieor S, Katzav-Gozansky T, Hefetz A (2008) Aggressive reproductive competition among hopelessly queenless honeybee workers triggered by pheromone signaling. Naturwissenschaften 95:553–559. doi: 10.1007/s00114-008-0358-z CrossRefPubMedGoogle Scholar
  23. Melathopoulos AP, Winston ML, Pettis JS, Pankiw T (1996) Effect of queen mandibular pheromone on initiation and maintenance of queen cells in the honey bee (Apis mellifera L.). Can Entomol 128:263–272CrossRefGoogle Scholar
  24. Mohammedi A, Paris A, Crauser D, Le Conte Y (1998) Effect of aliphatic esters on ovary development of queenless bees (Apis melliera L.). Naturwissenschaften 85:455–458. doi: 10.1007/s001140050531 CrossRefGoogle Scholar
  25. Moritz RFA, Crewe RM, Hepburn HR (2002) Queen avoidance and mandibular gland secretion of honeybee workers (Apis mellifera L.). Insectes Soc 49:86–91. doi: 10.1007/s00040-002-8284-0 CrossRefGoogle Scholar
  26. Naumann K, Winston ML, Slessor KN et al (1992) Intra-nest transmission of aromatic honey bee queen mandibular gland pheromone components: movement as a unit. Can Entomol 124:917–934CrossRefGoogle Scholar
  27. Naumann K, Winston ML, Slessor KN (1993) Movement of honey bee (Apis mellifera L.) queen mandibular gland pheromone in populous and unpopulous colonies. J Insect Behav 6:211–223. doi: 10.1007/BF01051505 CrossRefGoogle Scholar
  28. Oldroyd BP, Beekman M (2008) Effects of selection for honey bee worker reproduction on foraging traits. PLoS Biol 6, e56. doi: 10.1371/journal.pbio.0060056 PubMedCentralCrossRefPubMedGoogle Scholar
  29. Pankiw T (1997) Queen rearing by high and low queen mandibular pheromone responding worker honey bees (Apis mellifera L). Can Entomol 129:679–690CrossRefGoogle Scholar
  30. Paul RK, Takeuchi H, Kubo T (2006) Expression of two ecdysteroid-regulated genes, Broad-Complex and E75, in the brain and ovary of the honeybee (Apis mellifera L.). Zoolog Sci 23:1085–1092. doi: 10.2108/zsj.23.1085 CrossRefPubMedGoogle Scholar
  31. Pettis JS, Winston ML, Collins AM (1995) Suppression of queen rearing in European and Africanized honey bees Apis mellifera L. by synthetic queen mandibular gland pheromone. Insectes Soc 121:113–121CrossRefGoogle Scholar
  32. Pirk C, Boodhoo C, Human H, Nicolson S (2010) The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41:62–72. doi: 10.1051/apido/2009055 CrossRefGoogle Scholar
  33. Ratnieks FLW, Reeve HK (1992) Conflict in single-queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species.Google Scholar
  34. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608. doi: 10.1146/annurev.ento.51.110104.151003 CrossRefPubMedGoogle Scholar
  35. Roth KM, Beekman M, Allsopp MH et al (2014) Cheating workers with large activated ovaries avoid risky foraging. Behav Ecol 25:668–674. doi: 10.1093/beheco/aru043 CrossRefGoogle Scholar
  36. Seeley TD (1979) Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol 5:391–415. doi: 10.1007/BF00292527 CrossRefGoogle Scholar
  37. Slessor KN, Kaminski L-A, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356CrossRefGoogle Scholar
  38. Takeuchi H, Paul RK, Matsuzaka E, Kubo T (2007) EcR-A expression in the brain and ovary of the honeybee (Apis mellifera L.). Zoolog Sci 24:596–603. doi: 10.2108/zsj.24.596 CrossRefPubMedGoogle Scholar
  39. Tan K, Liu X, Dong S et al (2015) Pheromones affecting ovary activation and ovariole loss in the Asian honey bee Apis cerana. J Insect Physiol 74:25–29. doi: 10.1016/j.jinsphys.2015.01.006 CrossRefPubMedGoogle Scholar
  40. Velthuis HHW (1970) Ovarian development in Apis mellifera worker bees. Entomol Exp Appl 13:377–394. doi: 10.1007/BF00333492 CrossRefGoogle Scholar
  41. Vergoz V, McQuillan HJ, Geddes LH et al (2009) Peripheral modulation of worker bee responses to queen mandibular pheromone. Proc Natl Acad Sci U S A 106:20930–20935. doi: 10.1073/pnas.0907563106 PubMedCentralCrossRefPubMedGoogle Scholar
  42. Wang Y, Kaftanoglu O, Siegel AJ et al (2010) Surgically increased ovarian mass in the honey bee confirms link between reproductive physiology and worker behavior. J Insect Physiol 56:1816–1824. doi: 10.1016/j.jinsphys.2010.07.013 CrossRefPubMedGoogle Scholar
  43. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  44. Winston ML (1991) The biology of the honey bee, 1st edn. Harvard University PressGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Entomology, Center for Pollinator ResearchPennsylvania State UniversityUniversity ParkUSA
  2. 2.School of Life SciencesArizona State UniversityTempeUSA
  3. 3.Department of Chemistry, Biotechnology and Food ScienceNorwegian University of Life SciencesAkershusNorway

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