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Individual responsiveness to shock and colony-level aggression in honey bees: evidence for a genetic component

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Abstract

The phenotype of the social group is related to phenotypes of individuals that form that society. We examined how honey bee colony aggressiveness relates to individual response of male drones and foraging workers. Although the natural focus in colony aggression has been on the worker caste, the sterile females engaged in colony maintenance and defense, males carry the same genes. We measured aggressiveness scores of colonies and examined components of individual aggressive behavior in workers and haploid sons of workers from the same colony. We describe for the first time, that males, although they have no stinger, do bend their abdomen (abdominal flexion) in a posture similar to stinging behavior of workers in response to electric shock. Individual worker sting response and movement rates in response to shock were significantly correlated with colony scores. In the case of drones, sons of workers from the same colonies, abdominal flexion significantly correlated but their movement rates did not correlate with colony aggressiveness. Furthermore, the number of workers responding at increasing levels of voltage exhibits a threshold-like response, whereas the drones respond in increasing proportion to shock. We conclude that there are common and caste-specific components to aggressive behavior in honey bees. We discuss implications of these results on social and behavioral regulation and genetics of aggressive response.

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References

  • Abramson CI (1989) Aversive conditioning in honeybees (Apis mellifera). J Comp Psychol 100:108–116

    Article  Google Scholar 

  • Agarwal C, Giannoni Guzmán M, Morales-Matos C, Del Valle Díaz RA, Abarmson CI, Giray TG (2011) Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PLoS One 6:e25371. doi:10.1371/journal.pone.0025371

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alaux C, Robinson GE (2007) Alarm pheromone induces immediate-early gene expression and slow behavioral response in the honey bees. J Chem Ecol 33:1346–1350. doi:10.1007/s10886-007-9301-6

    Article  CAS  PubMed  Google Scholar 

  • Arechavaleta-Velasco ME, Hunt GJ (2004) Binary trait loci that influence honey bee (Hymenoptera: Apidae) guarding behavior. Ann Entomol Soc Am 97:177–183. doi:10.1603/0013-8746(2004)097[0177:BTLTIH]2.0.CO;2

    Article  CAS  Google Scholar 

  • Baldemarra N, Díaz H, Sequeda A, Núñez J, Maldonado H (1987) Behavioral and pharmacological analysis of the stinging response in Africanized and Italian bees. In: Mercer A, Menzel R (eds) Neurobiology and behavior of the honeybee, 1st edn. Springer-Verlag, Berlin Heidelberg, pp 121–128

    Chapter  Google Scholar 

  • Beye M, Hasselmann M, Fondrk MK, Page RE Jr, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee that encodes an SR-Type protein. Cell 114:419–429. doi:10.1016/S0092-8674(03)00606-8

    Article  CAS  PubMed  Google Scholar 

  • Bhagavan S, Benatar S, Cobey S, Smith BH (1994) Effect of genotype but not age or caste on olfactory learning performance in the honey bee, Apis mellifera. Anim Behav 48:1357–1369. doi:10.1006/anbe.1994.1372

    Article  Google Scholar 

  • Breed MD, Robinson GE, Page RE Jr (1990) Division of labor during honey bee colony defense. Behav Ecol Sociobiol 27:395–401. doi:10.1007/BF00164065

    Article  Google Scholar 

  • Breed MD, Guzman-Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298. doi:10.1146/annurev.ento.49.061802.123155

    Article  CAS  PubMed  Google Scholar 

  • Burrell BD, Smith BH (1994) Age- but not caste-related regulation of abdominal mechanisms underlying the sting reflex of the honey bee, Apis mellifera. J Comp Physiol A 174:581–592. doi:10.1007/BF00217379

    Article  Google Scholar 

  • Burrell BD, Smith BH (1995) Modulation of the honey bee (Apis mellifera) sting response by octopamine. J Insect Physiol 41:671–680. doi:10.1016/0022-1910(95)00022-M

    Article  CAS  Google Scholar 

  • Cargel RA, Rinderer TE (2006) Queen cell acceptance in laying worker colonies of Russian and Italian honey bees. Am Bee J 146:698–700

    Google Scholar 

  • Chapman TW, Crespi BJ, Kranz BD, Schwarz MP (1999) High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips. Proc Natl Acad Sci 97:1648–1650. doi:10.1073/pnas.020510097

    Article  Google Scholar 

  • Cingolani P, Cao X, Khetani RS, Chen CC, Coon M, Sammak A, Bollig-Fischer A, Land S, Huang Y, Hudson ME, Garfinkel MD, Zhong S, Robinson GE, Ruden DM (2013) Intronic Non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees. BMC Genomics 14:666. doi:10.1186/1471-2164-14

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collins AM, Rinderer TE, Harbo JR, Brown MA (1984) Heritabilities and correlations for several characters in the honey bee. J Hered 75:135–140

    Google Scholar 

  • Dinges CW, Avalos A, Abramson CI, Craig DPA, Austin ZM, Varnon CA, Dal FN, Giray T, Wells H (2013) Aversive conditioning in honey bees (Apis mellifera anatoliaca): a comparison of drones and workers. J Exp Biol 216:4124–4134. doi:10.1242/jeb.090100

    Article  PubMed  Google Scholar 

  • Evans HE, West-Eberhard MJ (1971) The wasps. University of Michigan Press, Michigan

    Google Scholar 

  • Fahrbach SE, Giray T, Farris SM, Robinson GE (1997) Expansion of the neuropil of the mushroom bodies in male honey bees is coincident with initiation of flight. Neurosci Lett 236:135–138. doi:10.1016/S0304-3940(97)00772-6

    Article  CAS  PubMed  Google Scholar 

  • Ferguson HJ, Cobey S, Smith BH (2001) Sensitivity to change in rewards is heritable in the honeybee, Apis mellifera. Anim Behav 61:527–534. doi:10.1006/anbe.2000.1635

    Article  Google Scholar 

  • Fu Y, Chen Y, Yao T, Li P, Ma Y, Wang J (2013) Effects of morphine on associative memory and locomotor activity in the honey bee (Apis mellifera). Neurosci Bull 29:270–278. doi:10.1007/s12264-013-1308-0

    Article  CAS  PubMed  Google Scholar 

  • Galindo-Cardona A, Monmany AC, Moreno-Jackson R, Rivera-Rivera C, Huertas-Dones C, Caicedo-Quiroga L, Giray T (2012) Landscape analysis of drone congregation areas of the honey bee, Apis mellifera. J Insect Sci 12:1–15. doi:10.1673/031.012.12201

  • Galindo-Cardona A, Rivera-Marchand B, Acevedo J, Giray T (2013) Genetic structure of the gentle Africanized honey bee population (gAHB) in Puerto Rico. BMC Genet 14:65. doi:10.1186/1471-2156-14-65

  • Giray T, Robinson GE (1996) Common endocrine and genetic mechanisms of behavioral development in male and worker honey bees and the evolution of division of labor. P Natl Acad Sci 93:11718–11722

    Article  CAS  Google Scholar 

  • Giray T, Guzman-Novoa E, Aron CW, Zelinsky B, Fahrbach SE, Robinson GE (2000) Genetic variation in worker temporal polyethism and colony defensiveness in the honey bee, Apis mellifera. Behav Ecol 11:44–55

    Article  Google Scholar 

  • Grüter C, Memezes C, Imperatriz-Fonseca VL, Ratnieks FLW (2011) A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee. P Natl Acad Sci 109:1182–1186. doi:10.1073/pnas.1113398109

    Article  Google Scholar 

  • Guzman-Novoa E, Page RE Jr (1999) Selective breeding of honey bees (Hymenoptera: Apidae) in Africanized areas. J Econ Entomol 92:521–525

    Google Scholar 

  • Guzman-Novoa E, Page RE Jr, Spangler HG, Erickson EH (1999) A comparison of two assay to test the defensive behavior of honey bees (Apis mellifera). J Apic Res 38:205–209

    Google Scholar 

  • Guzman-Novoa E, Hunt GJ, Uribe JL, Smith C, Arechavaleta-Velasco ME (2002) Confirmation of QTL effects and evidence of genetic dominance of honeybee defensive behavior: results of colony and individual behavioral assay. Behav Genet 32:95–102. doi:10.1023/A:1015245605670

    Google Scholar 

  • Guzman-Novoa E, Prieto-Merlos D, Uribe-Rubio JL, Hunt GJ (2003) Relative reliability of four field assays to test defensive behavior of honey bees (Apis mellifera). J Apic Res 42:42–46

    Google Scholar 

  • Guzman-Novoa E, Hunt GJ, Page RE Jr, Uribe-Rubio JL, Prietos-Merlos D, Becerra-Guzman F (2005) Paternal effects on the defensive behavior of honey bees. J Hered 96:376–380. doi:10.1093/jhered/esi038

    Google Scholar 

  • Haight KL, Tschinkel WR (2003) Patterns of venom synthesis and use in the fire ant, Solenopsis invicta. Toxicon 42:673–682. doi:10.1016/j.toxicon.2003.09.005

    Article  CAS  PubMed  Google Scholar 

  • Hunt GJ (2007) Flight and fight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior. J Insect Physiol 53:399–410. doi:10.1016/j.jinsphys.2007.01.010

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt GJ, Guzman-Novoa E, Fondrk MK, Page RE Jr (1998) Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148:1203–1213

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, Williams CE, Rueppell O, Guzmán-Novoa E, Arechavaleta-Velasco M, Chandra S, Fondrk MK, Beye M, Page RE Jr (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94:247–267. doi:10.1007/s00114-006-0183-1

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kolmes SA, Fergusson-Kolmes LA (1989) Stinging behavior and residual value of worker honey bees (Apis mellifera). J N Y Entomol Soc 97:218–231

    Google Scholar 

  • Kolmes SA, Njehu N (1990) Effect of queen mandibular pheromones on Apis mellifera worker stinging behavior (Hymenoptera: Apidae). J N Y Entomol Soc 98:495–498

    Google Scholar 

  • Lenoir JC, Laloi D, Dechaume-Moncharmont FX, Solignac M, Pham MH (2006) Intra-colonial variation of the sting extension response in the honey bee Apis mellifera. Insect Soc 53:80–85. doi:10.1007/s00040-005-0838-5

    Article  Google Scholar 

  • Morgenstern D, King GF (2013) The venom optimization hypothesis revisited. Toxicon 63:120–128. doi:10.1016/j.toxicon.2012.11.022

    Google Scholar 

  • Núñez JA, Maldonado H, Miralto A, Balderrama N (1983) The stinging response of the honeybee: effects of morphine naloxone and some opioid peptides. Pharmacol Biochem Behav 19:921–924

    Article  PubMed  Google Scholar 

  • Ogawa H, Kawakami Z, Yamaguchi T (1995) Motor pattern of the stinging response in the honeybee Apis mellifera. J Exp Biol 189:39–47

    Google Scholar 

  • Ogawa H, Kawakami Z, Yamaguchi T (2011) Proprioceptors involved in stinging response of the honeybee Apis mellifera. J Insect Physiol 57:1358–1367. doi:10.1016/j.jinsphys.2011.07.003

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria. ISBN 3-900051-07-0 URL http://www.R-project.org

  • Rivera-Marchand B, Giray T, Guzman-Novoa E (2008) The cost of defense in social insects: insights from the honey bee. Entomol Exp Appl 129:1–10. doi:10.1111/j.1570-7458.2008.00747.x

    Google Scholar 

  • Rivera-Marchand B, Oskay D, Giray T (2012) Gentle Africanized bees on an oceanic island. Evol Appl 5:745–756. doi:10.1111/j.1752-4571.2012.00252.x

    Google Scholar 

  • Robinson GE (1997) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J Comp Physiol 160:613–619

    Article  Google Scholar 

  • Robinson GE, Page RE Jr (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358

    Article  Google Scholar 

  • Robinson GE, Grozinger CM, Whitfield CW (2005) Sociogenomics: social life in molecular terms. Nat Rev 6:257–270. doi:10.1038/nrg1575

    Article  CAS  Google Scholar 

  • Roussel E, Carcaud J, Sandoz JC, Giurfa M (2009) Reappraising social insect behavior through aversive responsiveness and learning. PLoS One 4:e4197. doi:10.1371/journal.pone.0004197

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roux EA, Korb J (2004) Evolution of eusociality and the soldier caste in termites: a validation of the intrinsic benefit hypothesis. J Evol Biol 17:869–875. doi:10.1111/j.1420-9101.2004.00727.x

    Article  CAS  PubMed  Google Scholar 

  • Schneider SS, DeGrandi-Hoffman G, Smith DR (2004) The African honey bee: factors contributing to a successful biological invasion. Annu Rev Entomol 49:351–376. doi:10.1146/annurev.ento.49.061802.123359

    Article  CAS  Google Scholar 

  • Shorter JR, Rueppell O (2012) A review on self-destructive defense behaviors in social insects. Insect Soc 59:1–10. doi:10.1007/s00040-011-0210-x

    Article  Google Scholar 

  • Spangler HG, Sprenkle DJ (1997) An instrument for quantifying honey bee defensiveness. Appl Acoust 50:325–332

    Article  Google Scholar 

  • Starr CK (1981) Defensive tactics of social wasps. Dissertation, University of Georgia, Athens

    Google Scholar 

  • Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev 71:27–79

    Article  CAS  PubMed  Google Scholar 

  • Stiles EW (1979) Evolution of color pattern and pubescence characteristics in male bumblebees: automimicry vs. thermoregulation. Evolution 33:941–957

    Article  Google Scholar 

  • Tedjakumala SR, Giurfa M (2013) Rules and mechanisms of punishment learning in honey bees: the aversive conditioning of the sting extension response. J Exp Biol 216:2985–2997. doi:10.1242/jeb.086629

    Article  PubMed  Google Scholar 

  • Tel-Zur D, Lensky Y (1995) Bioassay and apparatus for measuring the stinging response of an isolated worker honey-bee (Apis mellifera L. var lingustica Spin.). Comp Biochem Physiol A 110:281–288

    Article  Google Scholar 

  • Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. P Natl Acad Sci 100:12808–12813. doi:10.1073/pnas.2133530100

    Article  CAS  Google Scholar 

  • Tóth E, Duffy JE (2008) Influence of sociality on allometric growth and morphological differentiation in sponge dwelling alpheid shrimp. Biol J Linn Soc 94:527–540. doi:10.1111/j.1095-8312.2008.01013.x

    Article  Google Scholar 

  • Urlacher E, Francés B, Giurfa M, Devaud JM (2010) An alarm pheromone modulates appetitive olfactory learning in the honeybee (Apis mellifera). Front Behav Neurosci 4:157. doi:10.3389/fnbeh.2010.00157

    PubMed Central  PubMed  Google Scholar 

  • Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 3:e288. doi:10.1371/journal.pone.0000288

    Article  Google Scholar 

  • Vetter RS, Visscher PK (1997) Influence of age on antennal response of male honey bees Apis mellifera to queen mandibular pheromone and alarm pheromone component. J Chem Ecol 23:1867–1880

    Article  CAS  Google Scholar 

  • Wheeler DE (1991) The developmental basis of worker caste polymorphism in ants. Am Nat 138:1218–1238

    Article  Google Scholar 

  • Whitfield CW, Band MR, Bonaldo MF, Kumar CG, Liu L, Pardinas JR, Robertson HM, Soares MB, Robinson GE (2002) Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res 12:555–566. doi:10.1101/gr.5302

    Article  PubMed Central  PubMed  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, MA

    Google Scholar 

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Acknowledgments

Research was conducted with funds from a USDA-NIFA award (2009-05291) to TG, the NSF-REU program (1156810) to YRC, and the RISE Graduate Fellowship Program (R25GM061151-11) to AA. We like to thank Dr. Gene E. Robinson for his suggestions during project development. We also thank Dr. Jose L. Agosto, Manuel Giannoni-Guzmán, and the BIOL6990-Behavioral Plasticity Seminar course members for taking the time to provide revisions and critiques. We appreciate and thank Dr. Alberto Galindo for his insight and assistance, Dr. Charles I Abramson for his constructive criticism and help with the language and exposition of the manuscript, and Dr. María Eglée Pérez for statistical revision and assistance. Further thanks to Gabriel Diaz our apiary technician whose assistance was essential for project coordination.

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Correspondence to Arian Avalos.

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Communicated by M. Giurfa

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Worker and drone behaviors. Pictures illustrating similarities of worker stinging behavior (a) and drone abdomen flexion (b) (GIF 535 kb)

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Electric shock assay. Video sample of worker sting and drone abdomen flexion in response to electric shock under assay conditions (MPG 3472 kb)

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Avalos, A., Rodríguez-Cruz, Y. & Giray, T. Individual responsiveness to shock and colony-level aggression in honey bees: evidence for a genetic component. Behav Ecol Sociobiol 68, 761–771 (2014). https://doi.org/10.1007/s00265-014-1689-8

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