Skip to main content
Log in

Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.)

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

Abstract

There have been numerous reports of genetic influences on division of labor in honey bee colonies, but the effects of worker genotypic diversity on colony behavior are unclear. We analyzed the effects of worker genotypic diversity on the phenotypes of honey bee colonies during a critical phase of colony development, the “nest initiation” phase. Five groups of colonies were studied (n = 5–11 per group); four groups had relatively low genotypic diversity compared to the fifth group. Colonies were derived from queens that were instrumentally inseminated with the semen of four different drones according to one of the following mating schemes: group A, 4 A-source drones; group B, 4 B-source drones; group C, 4 C-source drones; group D, 4 D-source drones; and group E, 1 drone of each of the A-D drone sources. There were significant differences between colonies in groups A-D for 8 out of 19 colony traits. Because the queens in all of these colonies were super sisters, the observed differences between groups were primarily a consequence of differences in worker genotypes. There were very few differences (2 out of 19 traits) between colonies with high worker genotypic diversity (group E) and those with low diversity (groups A-D combined). This is because colonies with greater diversity tended to have phenotypes that were average relative to colonies with low genotypic diversity. We hypothesize that the averaging effect of genotypic variability on colony phenotypes may have selective advantages, making colonies less likely to “fail” because of inappropriate colony responses to changing environmental conditions.

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.

Similar content being viewed by others

References

  • Bailey L, Ball BV (1991) honey bee pathology. Academic Press, London

    Google Scholar 

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

    Google Scholar 

  • Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialisation in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17–25

    Google Scholar 

  • Calderone NW, Page RE (1991) The evolutionary genetics of division of labor in colonies of the honey bee (Apis mellifera). Am Nat 138:69–92

    Google Scholar 

  • Calderone NW, Page RE (1992) Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera). Behav Ecol Sociobiol 30:219–226

    Google Scholar 

  • Calderone NW, Robinson GE, Page RE (1989) Genetic structure and division of labor in honeybee societies. Experientia 45: 765–767

    Google Scholar 

  • Camazine S (1993) The regulation of pollen foraging by honey bees: how foragers assess the colony's need for pollen. Behav Ecol Sociobiol 32:265–272

    Google Scholar 

  • Carlin NF, Reeve HK, Cover SP (1993) Kin discrimination and division of labor among matrilines in the polygynous carpenter ant, Camponotus planatus. In: Keller L (ed) queen number and sociality in insects. Oxford University Press, Oxford, pp 362–401

    Google Scholar 

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

    Google Scholar 

  • Collins AM (1986) Bidirectional selection for colony defense in Africanized honey bees. Am Bee J 126:827–828

    Google Scholar 

  • Collins AM, Rinderer TE, Harbo JR, Bolton AB (1982) Colony defense by Africanized and European honey bees. Science 218: 72–74

    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 

  • Collins AM, Rinderer TE, Tucker K (1988) Colony defence of two honeybee types and their hybrids. I. Naturally mated queens. J Apic Res 27:137–140

    Google Scholar 

  • Crozier RH, Consul PC (1976) Conditions for genetic polymorphisms in social Hymenoptera under selection at the colony level. Theor Popul Biol 10:1–9

    Google Scholar 

  • Crozier RH, Page RE (1985) On being the right size: male contributions and multiple mating in social Hymenoptera. Behav Ecol Sociobiol 18:105–115

    Google Scholar 

  • Fewell JH, Page RE (1993) Genotypic variation in foraging responses to environmental stimuli by honey bees, Apis mellifera. Experientia 49:1106–1112

    Google Scholar 

  • Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol 30:387–394

    Google Scholar 

  • Frumhoff PC, Baker J (1988) A genetic component to division of labour within honey bee colonies. Nature 333:358–361

    Google Scholar 

  • Fuchs S, Schade V (1994) Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155–168

    Google Scholar 

  • Gary NE, Lorenzen K (1984) Improved trap to recover dead and abnormal honey bees (Hymenoptera: Apidae) from hives. J Econ Entomol 13:718–723

    Google Scholar 

  • Gilliam M, Taber S, Richardson GV (1984) Hygienic behavior of honey bees in relation to chalkbrood disease. Apidologie 14: 29–39

    Google Scholar 

  • Giray T, Robinson GE (1994) Genetic variability for behavioral development and plasticity of age polyethism in honey bee colonies. Behav Ecol Sociobiol 35:13–20

    Google Scholar 

  • Guzmán-Novoa E, Page RE (1993) Backcrossing Africanized honey bee queens to European drones reduces colony defensive behavior. Ann Entomol Soc Am 86:352–355

    Google Scholar 

  • Guzmán-Novoa E, Page RE (1994) Genetic dominance and worker interactions affect honey bee colony defense. Behav Ecol 5:91–97

    Google Scholar 

  • Guzmán-Novoa E, Page RE, Gary NE (1994) Behavioral and life history components of division of labor in honey bees (Apis mellifera L.). Behav Ecol Sociobiol 34:409–417

    Google Scholar 

  • Kauffeld N (1975) Overwintering of colonies of honey bees with restricted and unrestricted broodrearing in Louisiana. Am Bee J 115:480–481, 490

    Google Scholar 

  • Kauffman SA (1991) Antichaos and adaptation. Sci Am 265:78–84

    Google Scholar 

  • Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704

    Google Scholar 

  • Kolmes SA, Winston ML, Fergusson LA (1989) The division of labor among worker honey bees (Hymenoptera: Apidae): the effects of multiple patrilines. J Kans Entomol Soc 62:80–95

    Google Scholar 

  • Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honey bees (Apis mellifera capensis Esch.). Behav Ecol Sociobiol 17:87–89

    Google Scholar 

  • Moritz RFA, Southwick EE (1987) Phenotype interactions in group behavior of honey bee workers (Apis mellifera L.). Behav Ecol Sociobiol 21:53–57

    Google Scholar 

  • Moritz RFA, Southwick EE (1993) Bees as superorganisms: an evolutionary reality. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Oldroyd BP, Rinderer TE, Buco SM (1992a) Intra-colonial foraging specialism by honey bees (Apis mellifera). Behav Ecol Sociobiol 30:291–295

    Google Scholar 

  • Oldroyd BP, Rinderer TE, Harbo JR, Buco SM (1992b) Effects of intracolonial genetic diversity on honey bee (Hymenopotera: Apidae) colony performance. Ann Entomol Soc Am 85:335–343

    Google Scholar 

  • Oldroyd BP, Rinderer TE, Buco SM, Beaman LD (1993) Genetic variance in honey bees for preferred foraging distance. Anim Behav 45:323–332

    Google Scholar 

  • Oldroyd BP, Sylvester HA, Wongsiri S, Rinderer TE (1994) Task specialization in a wild bee, Apis florea (Hymenoptera: Apidae), revealed by RFLP banding. Behav Ecol Sociobiol 34:25–30

    Google Scholar 

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

    Google Scholar 

  • Page RE, Laidlaw HH (1988) Full sisters and super sisters: a terminological paradigm. Anim Behav 36:944–945

    Google Scholar 

  • Page RE, Metcalf RA (1984) A population investment sex ratio for the honey bee (Apis mellifera L.). Am Nat 124:680–702

    Google Scholar 

  • Page RE, Mitchell SD (1991) Self organization and adaptation in social insects. In: Fine A, Forbes M, Wessels L (eds) PSA 1990 2. Philosophy of Science Association, East Lansing, Michigan, pp 289–298

    Google Scholar 

  • Page RE, Robinson GE (1991) The genetics of division of labour in honey bee colonies. Adv Insect Physiol 23:118–169

    Google Scholar 

  • Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition, and nepotism in honey-bee colonies. Nature 338:576–579

    Google Scholar 

  • Page RE, Robinson GE, Britton DS, Fondrk MK (1992) Genotypic variability for rates of development in worker honey bees (Apis mellifera). Behav Ecol 3:173–180

    Google Scholar 

  • Page RE, Fondrk MK, Robinson GE (1993) Selectable components of sex allocation in colonies of the honey bee (Apis mellifera L.). Behav Ecol 4:239–245

    Google Scholar 

  • Pamilo P, Crozier RH (1982) Measuring genetic relatedness in natural populations: methodology. Theor Popul Biol 21:171–193

    Google Scholar 

  • Ratnieks FLW (1990) The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males. Behav Ecol Sociobiol 26:343–348

    Google Scholar 

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

    Google Scholar 

  • Robinson GE, Page RE (1989a) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol 24:317–323

    Google Scholar 

  • Robinson GE, Page RE (1989b) Genetic basis for division of labor in an insect society. In: Breed MD Breed, Page RE (eds), The genetics of social evolution. Westview Press, Boulder, pp. 61–80

    Google Scholar 

  • Robinson GE, Page RE (in press) Genotypic constraints on plasticity for corpse removal in honey bee colonies. Anim Behav

  • Robinson GE, Page RE, Arensen N (1994) Genotypic differences in brood rearing in honey bee colonies: context-specific? Behav Ecol Sociobiol 34:125–137

    Google Scholar 

  • Robinson GE, Page RE, Strambi C, Strambi A (1989) Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246:109–112

    Google Scholar 

  • Robinson GE, Page RE, Fondrk MK (1990) Intracolonial behavioral variation in worker oviposition, oophagy, and larval care in queenless honey bee colonies. Behav Ecol Sociobiol 26: 315–323

    Google Scholar 

  • Rothenbuhler WC (1964) Behavioral genetics of nest cleaning in honey bees, IV. Responses of F2 and backcross generations to disease-killed brood. Am Zool 4:111–123

    Google Scholar 

  • Sakagami S, Fukuda H (1968) Life tables for worker honeybees. Res Popul Ecol 10:127–139

    Google Scholar 

  • Schmidt JO, Buchmann SL (1992) Other products of the hive. In: Graham JM (ed) The hive and the honey bee. Dadant, Hamilton, Illinois, pp. 927–988

    Google Scholar 

  • Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293

    Google Scholar 

  • Seeley TD (1985) Honeybee ecology: A study of adaptation in social life.Princeton University Press, Princeton

    Google Scholar 

  • Seeley TD, Morse RA (1976) The nest of the honey bee (Apis mellifera L.). Insectes Soc 23:495–512

    Google Scholar 

  • Seeley TD, Visscher PK (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol 10:81–88

    Google Scholar 

  • Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in the social Hymenoptera. Am Nat 131:602–610

    Google Scholar 

  • Snyder LE (1992) The genetics of social behavior in a polygynous ant. Naturwissenschaften 79:525–527

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry Freeman, New York

    Google Scholar 

  • Stort AC (1974) Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. I. Some tests to measure aggressiveness. J Apic Res 13:33–38

    Google Scholar 

  • Stort AC (1975a) Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. II. Time at which the first sting reached the leather ball. J Apic Res 14:171–175

    Google Scholar 

  • Stort AC (1975b) Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. IV. Number of stings in the gloves of the observer. Behav Genet 5:269–274

    Google Scholar 

  • Stort AC (1975c) Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. V. Number of stings in the leather ball. J Kans Entomol Soc 48:381–387

    Google Scholar 

  • Stuart RJ, Page RE (1991) Genetic component to division of labor among workers of a leptothoracine ant. Naturwissenschaften 78:375–377

    Google Scholar 

  • Visscher PK (1983) The honey bee way of death: necrophoric behavior in Apis mellifera colonies. Anim Behav 31:1070–1076

    Google Scholar 

  • Villa JD (1988) Defensive behaviour of Africanized and European honeybees at two elevations in Colombia. J Apic Res 27:141–145

    Google Scholar 

  • Wilkinson L (1989) Systat: the system for statistics. Systat, Evanston

    Google Scholar 

  • Winston ML (1980) Swarming, after swarming, and reproductive rate of unmanaged honeybee colonies (Apis mellifera). Insectes Soc 27:391–398

    Google Scholar 

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

    Google Scholar 

  • Woyke J (1986) Sex determination. In: Rinderer TE (ed), Bee genetics and breeding, Academic Press, Orlando, pp 91–119

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by P. Pamilo

Rights and permissions

Reprints and permissions

About this article

Cite this article

Page, R.E., Robinson, G.E., Fondrk, M.K. et al. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36, 387–396 (1995). https://doi.org/10.1007/BF00177334

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00177334

Key words

Navigation