Skip to main content
Log in

Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

There has now been an abundance of research conducted to explore genetic bases that underlie learning performance in the honey bee (Apis mellifera). This work has progressed to the point where studies now seek to relate genetic traits that underlie learning ability to learning in field-based foraging problems faced by workers. Accordingly, the focus of our research is to explore the correlation between laboratory-based performance using an established learning paradigm and field-based foraging behavior. To evaluate learning ability, selected lines were established by evaluating queens and drones in a proboscis extension reflex (PER) conditioning procedure to measure learning in a laboratory paradigm—latent inhibition (LI). Hybrid queens were then produced from our lines selected for high and low levels of LI and inseminated with semen from many drones chosen at random. The genetically diverse worker progeny were then evaluated for expression of LI and for preference of pollen and/or nectar during foraging. Foragers from several different queens, and which had resulted from fertilization by any of several different drone fathers, were collected as they returned from foraging flights and analyzed for pollen and nectar contents. They were subsequently evaluated for expression of LI. Our research revealed that pollen foragers exhibited stronger learning, both in the presence (excitatory conditioning) and absence (LI) of reinforcement. The heightened overall learning ability demonstrated by pollen foragers suggests that pollen foragers are in general more sensitive to a large number of environmental stimuli. This mechanism could contribute toward explanations of colony-level regulation of foraging patterns among workers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a-f
Fig. 2a-c
Fig. 3

Similar content being viewed by others

References

  • Benatar ST, Cobey S, Smith BH (1995) Selection on haploid genotype for discrimination learning performance: Correlation between drone honey bees (Apis mellifera) and their worker progeny (Hymenoptera: Apidae). J Insect Behav 8:637–652

    Google Scholar 

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

    Google Scholar 

  • Bitterman ME, Menzel R., Fietz A, Schafer S (1983) Classical conditioning of proboscis extension in honeybees, Apis mellifera. J Comp Psych 97:107–119

    Article  CAS  PubMed  Google Scholar 

  • Brandes C, Menzel R (1990) Common Mechanisms in proboscis extension conditioning and visual learning revealed by genetic selection in honey bees (Apis mellifera capensis). J Comp Physiol A 166:545–552

    Google Scholar 

  • Chandra BC, Hosler JS, Smith BH (2000) Heritable variation for latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera). J Comp Psych 114:86–97

    Google Scholar 

  • Chandra BC, Hunt GJ, Cobey S, Smith BH (2001) Quantitative trait loci associated with reversal learning and latent inhibition in honeybees (Apis mellifera). Behav Gen 31:275–285

    Google Scholar 

  • Dyer FC (1991) Bees acquire route-based memories but not cognitive maps in a familiar landscape. Anim Behav 4:239–246

    Google Scholar 

  • Eckert CD, Winston ML, Ydenberg RC (1994) The relationship between population size, amount of brood, and individual foraging behaviour in the honey bee, Apis mellifera L. Oecologia 97:248–255

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Addison Wesley Longman, London

  • Ferguson HJ, Cobey S, Smith BH (2001) Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera. Anim Behav 61:527–534

    Google Scholar 

  • Gary NE, Lorenzen K (1976) A method for collecting the honey sac contents from honeybess. J Apic Res 15:73–79

    Google Scholar 

  • Gould JL (1986) Pattern learning by honey bees. Anim Behav 34:990–997

    Google Scholar 

  • Greenspan RJ (2001) The flexible genome. Nature Rev Genet 2:383–387

    Google Scholar 

  • Hellmich RL, Kulincevic JM, Rothenbuhler WC (1985) Selection for high and low pollen-hoarding honey bees. J Hered 76:155–158

    Google Scholar 

  • Kevan PG (1987) Texture sensitivity in the life of honeybees. In: Menzel R, Mercer A (eds.) Neurobiology and behavior of honeybees. Springer, Berlin Heidelberg New York, pp 96–101

  • Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas, Cheshire, Conn.

  • Mackensen O, Nye WP, (1966) Selecting and breeding honey bees for the collecting of alfalfa pollen. J Apic Res 5:79–86

    Google Scholar 

  • Menzel R (1990) Learning, memory, and “cognition” honey bees. In: Kesner RP, Olten DS (eds) Neurobiology of comparative cognition. Erlbaum, Hillsdale, N.J., pp 237–292

  • Oster GF, Wilson EO, (1978) Social insects. Princeton University Press, Princeton, N.J.

  • Page RE (1986) Sperm utilization in social insects. Annu Rev Entomol 31:297–320

    Google Scholar 

  • Page RE, Fondrk MK (1995) The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.): colony-level components of pollen hoarding. Behav Ecol Sociobiol 36:135–144

    Google Scholar 

  • Page RE, Laidlaw HH (1982) Closed population honey bee breeding. I. Population genetics of sex determination. J Apic Res. 21:30–37

    Google Scholar 

  • Page RE, Robinson GE, (1991) The genetics of division of labor in honey bee colonies. In: Evans PD (ed) Advances in insect physiology, vol 23. Academic Press, London, pp 117–169

  • Page RE, Robinson GE, Fondrk MK, Nasr ME (1995a) Effects of genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396

    Google Scholar 

  • Page RE, Waddington KE, Hunt GJ, Fondrk MK (1995b) Genetic determinants of honey bee foraging behaviour. Anim Behav 50:1617–1625

    Google Scholar 

  • Page RE, Erber J, Fondrk MK (1998) The effect of genotype on the response thresholds to sucrose and foraging of honey bees (Apis mellifera L.). J Comp Physiol 182:489–500

    Article  PubMed  Google Scholar 

  • Pankiw T, Page RE (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L). J Comp Physiol 185:207–213.

    Article  CAS  PubMed  Google Scholar 

  • Rescorla RA (1988) Behavioral studies of Pavlovian conditioning. Annu Rev Neurosci 11:329–352

    Google Scholar 

  • Rothenbuhler WC, Kulincevic JM, Thompson VC (1979) Successful selection of honeybees for fast and slow hoarding of sugar syrup in the laboratory. J Apic Res 18:272–278

    Google Scholar 

  • Seeley TD (1985) Honeybee ecology. Princeton University Press, Princeton, N.J.

  • Scheiner R, Page RE, Erber J (2001a) Responsiveness to sucrose affects tactile and olfactory learning in honey bees of two genetic strains. Behav Brain Res 120:67–73

    Google Scholar 

  • Scheiner R, Page RE, Erber J (2001b) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem 76:138–150

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P, Kacelnik A, Houston AI, (1985) Honeybees maximize efficiency by not filling their crop. Behav Ecol Sociobiol 17:61–66

    Google Scholar 

  • Shafir S, Waite TA, Smith BH, (2002) Context dependent violations of rational choice in honeybees (Apis mellifera) and gray jays (Perisoreus canadensis). Behav Ecol Sociobiol 51:180–187

    Google Scholar 

  • Von Frisch K (1967) The dance language and orientation of honey bees. Harvard University Press, Cambridge, Mass.

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

Download references

Acknowledgements

This work was supported by NIH Grant 9 RO1 RR14166 to B.H.S. from NCRR. The authors wish to thank Susan Cobey and Sathees Chandra for assistance in aspects of fieldwork and laboratory analyses. The described experiments comply with current guidelines and regulations concerning subject handling.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brian H. Smith.

Additional information

Communicated by R. Page

Rights and permissions

Reprints and permissions

About this article

Cite this article

Latshaw, J.S., Smith, B.H. Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera). Behav Ecol Sociobiol 58, 200–207 (2005). https://doi.org/10.1007/s00265-004-0904-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0904-4

Keywords

Navigation