Behavioral Ecology and Sociobiology

, Volume 35, Issue 2, pp 99–107

Reproductive competition in queenless honey bee colonies (Apis mellifera L.)

  • Robert E. PageJr.
  • Gene E. Robinson


Previously we reported that there are subfamily differences in drone production in queenless honey bee colonies, but these biases are not always explained by subfamily differences in oviposition behavior. Here we determine whether these puzzling results are best explained by either inadequate sampling of the laying worker population or reproductive conflict among workers resulting in differential treatment of eggs and larvae. Using colonies composed of workers from electrophoretically distinct subfamilies, we collected samples of adult bees engaged in the following behavior: “true” egg laying, “false” egg laying, indeterminate egg laying, egg cannibalism, or nursing (contact with larvae). We also collected samples of drone brood at four different ages: 0 to 2.5-h-old eggs, 0 to 24-h-old eggs, 3 to 8-day-old larvae, and 9 to 14-day-old larvae and pupae. Allozyme analyses revealed significant subfamily differences in the likelihood of exhibiting egg laying, egg cannibalism, and nursing behavior, as well as significant subfamily differences in drone production. There were no subfamily differences among the different types of laying workers collected from each colony, suggesting that discrepancies between subfamily biases in egg-laying behavior and drone production are not due to inadequate sampling of the laying worker population. Subfamily biases in drone brood production within a colony changed significantly with brood age. Laying workers had significantly more developed ovaries than either egg cannibals or nurses, establishing a physiological correlate for the observed behavioral genetic differences. These results suggest there is reproductive conflict among subfamilies and individuals within queenless colonies of honey bees. The implications of these results for the evolution of reproductive conflict, in both queenright and queenless contexts, are discussed.

Key words

Apis mellifera Genetics Drone production Allozymes Reproductive conflict 


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  1. Adams J, Rothman ED, Kerr WE, Paulino ZL (1977) Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86:583–596Google Scholar
  2. Bailey L, Ball BV (1991) Honey bee pathology. Academic Press, LondonGoogle Scholar
  3. Breed MD, Butler L, Stiller T (1985) Kin recognition by worker honey bees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061PubMedGoogle Scholar
  4. Campbell DT (1983) The two distinct routes beyond kin selection to ultrasociality: implications for the humanities and social sciences. In: Bridgeman D (ed) The nature of prosocial development: theories and strategies. Academic Press, New York, pp 11–41Google Scholar
  5. Carlin NF, Frumhoff PC (1990) Nepotism in the honey bee. Nature 346:706–707Google Scholar
  6. Coelho JR, Mitton JB (1988) Oxygen consumption duing hovering is associated with genetic variation of enzymes in honey bees. Funct Ecol 2:141–146Google Scholar
  7. Contel EPB, Mestriner MA, Martins E (1977) Genetic control and developmental expression of malate dehydrogenase in Apis mellifera. Biochem Genet 15:859–876Google Scholar
  8. Delaplane KS, Harbo JR (1987) Drone production by young versus old worker honeybees in queenless colonies. Apidologie 18:115–120Google Scholar
  9. Engels W Imperatriz-Fonseca VL (1990) Caste development, reproductive strategies, and control of fertility in honey bees and stingless bees. In: Engels W (ed) Social insects. Springer, Berlin Heidelberg New York, pp 167–230Google Scholar
  10. Evers CA, Seeley TD (1986) Kin discrimination and aggression in honey bee colonies with laying workers. Anim Behav 34:924–944Google Scholar
  11. Free JB, Williams IH (1974) Factors determining food storage and brood rearing in honeybee (Apis mellifera L.) comb. J Entomol A 49:47–63Google Scholar
  12. Frumhoff PC, Schneider S (1987) The social consequences of honey bee polyandry: the effects of kinship on worker interactions within colonies. Anim Behav 35:255–262Google Scholar
  13. Getz WM, Smith KB (1983) Genetic kin recognition: honey bees discriminate between full and half sisters. Nature 302:147–148Google Scholar
  14. Hamilton WD (1964a) The genetical theory of social behavior I. J Theor Biol 7:1–16PubMedGoogle Scholar
  15. Hamilton WD (1964b) The genetical theory of social behavior II. J Theor Biol 7:17–52PubMedGoogle Scholar
  16. Hebert PDN, Beaton MJ (1989) Practical handbook of cellulose acetate gel electophoresis. Helena Labs, Beaumont, TexasGoogle Scholar
  17. Lindauer M (1953) Division of labor in the honeybee colony. Bee World 34:63–73, 85–90Google Scholar
  18. Mackensen O, Tucker KW (1970) Instrumental insemination of queen bees (Agricultural Handbook No. 390) US Government Printing Office, Washington, D.C.Google Scholar
  19. Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis Esch.). Behav Ecol Sociobiol 17:87–89Google Scholar
  20. Moritz RFA, Southwick EE (1992) Bees as superorganisms: an evolutionary reality. Springer, Berlin Heidelberg New YorkGoogle Scholar
  21. Noonan KC (1986) Recognition of queen larvae by worker honey bees (Apis mellifera). Ethology 73:295–306Google Scholar
  22. Noonan KC, Kolmes SA (1989) Kin recognition of worker brood by worker honey bees, Apis mellifera L. J Insect Behav 4:473–485Google Scholar
  23. Oldroyd BP, Rinderer TE, Buco SM (1990) Nepotism in the honey bee. Nature 346:707–708Google Scholar
  24. Page RE (1986) Sperm utilization in social insects. Annu Rev Entomol 31:297–320Google Scholar
  25. Page RE, Erickson EH (1984) Selective rearing of queens by worker honey bees: kin or nestmate recognition. Ann Entomol Soc Am 77:578–580Google Scholar
  26. Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera L.). Behav Ecol Sociobiol 23:117–126Google Scholar
  27. Page RE, Laidlaw HH (1988) Full sisters and super sisters: a terminological paradigm. Anim Behav 36:944–945Google Scholar
  28. Page RE, Metcalf RA (1984) A population investment sex ratio for the honey bee (Apis mellifera L.) Am Nat 124:680–702Google Scholar
  29. Page RE, Robinson GE (1990) Nepotism in the honey bee. Nature 346:708Google Scholar
  30. Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition, and nepotism in honey-bee colonies. Nature 338:576–579Google Scholar
  31. Page RE, Breed MD, Getz WM (1990) Nepotism in the honey bee. Nature 346:707Google Scholar
  32. Pamilo P, Crozier RH (1982) Measuring genetic relatedness in natural populations: methodology. Theor Popul Biol 21:171–193Google Scholar
  33. Plettner E, Slessor KN, Winston ML, Robinson GE, Page RE (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L.). J Insect Physiol 39:235–240Google Scholar
  34. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  35. Ratnieks FLW (1993) Egg laying, egg removal and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198Google Scholar
  36. Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797Google Scholar
  37. Robinson GE, Page RE (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358Google Scholar
  38. Robinson GE, Page RE, Strambi A, Strambi C (1989) Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246:109–112Google Scholar
  39. 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 26:315–323Google Scholar
  40. Ruttner F, Hesse B (1981) Rassenspezifische Unterschiede in Ovarentwicklung und Eiblage von weisellosen Arbeiterinnen der Honigbiene Apis mellifera L. Apidologie 12:159–183Google Scholar
  41. Sakagami SF (1954) Occurrence of an aggressive behavior in queenless hives, with considerations on the social organization of honeybees. Insectes Soc 1:221–343Google Scholar
  42. Sakagami SF (1958) The false queen: fourth adjustive response in dequeened honeybee colonies. Behaviour 13:280–295Google Scholar
  43. Sokal RR, Rohlf FJ (1981) Biometry. Freeman,San FranciscoGoogle Scholar
  44. Velthuis HHW (1970) Ovarian Development in Apis mellifera worker bees. Entomol Exp Appl 13:377–394Google Scholar
  45. Velthuis HHW (1985) The honeybee queen and the social organization of her colony. In: Holldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Sinauer, SunderlandGoogle Scholar
  46. Visscher PK (1986) Kinship discrimination in queen rearing by honey bees (Apis mellifera). Behav Ecol Sociobiol 18:453–460Google Scholar
  47. Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254Google Scholar
  48. Visscher PK (1990) Kin recognition and nepotism in Apis mellifera. In: Veeresh GK, Mallik B, Viraktamath CA (eds) Social insects and the environment. Oxford and IBH, New Delhi, pp 139–140Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Robert E. PageJr.
    • 1
  • Gene E. Robinson
    • 2
  1. 1.Department of EntomologyUniversity of CaliforniaDavisUSA
  2. 2.G.E. Robinson Department of EntomologyUniversity of IllinoisUrbanaUSA

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