Behavioral Ecology and Sociobiology

, Volume 26, Issue 5, pp 315–323 | Cite as

Intracolonial behavioral variation in worker oviposition, oophagy, and larval care in queenless honey bee colonies

  • Gene E. Robinson
  • Robert E. PageJr.
  • M. Kim Fondrk
Article

Summary

Two experiments were performed to determine whether worker reproduction in queenless honey bee colonies is influenced by colony genetic structure. In Experiment 1, allozyme analyses of workers and worker-derived drone larvae revealed that in half the colonies, there were genotypic differences in worker egg-laying behavior (presumed to involve actual oviposition), but biases in drone production were not always consistent with biases in egg-laying behavior. In Experiment 2, allozyme analyses again revealed intracolonial differences in egg-laying behavior and in behavior patterns thought to involve oophagy and larval care. Data support the hypothesis of a genetic influence on this intracolonial behavioral variation. Differences in the genotypic distributions of worker-derived drones relative to workers engaged in oviposition behavior in queenless colonies may be a consequence of genetic variability for egg production or for treatment of eggs and larvae (possibly coupled with kin recognition), or both.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  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. Boch R, Morse RA (1982) Genetic factor in queen recognition odors of honey bees. Ann Entomol Soc Am 75:654–656Google Scholar
  3. Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Quart Rev Biol 63:291–311Google Scholar
  4. Breed MD (1981) Individual recognition and learning of queen odors by worker honeybees. Proc Natl Acad Sci USA 78:2635–2637Google Scholar
  5. Breed MD (1983) Nestmate recognition in honey bees. Anim Behav 31:86–91Google Scholar
  6. Breed MD, Butler L, Stiller TM (1985) Kin recognition by worker honey bees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061Google Scholar
  7. Burgett M, Burikam I (1985) Number of adult honey bees (Hymenoptera: Apidae) occupying a comb: a standard for estimating colony populations. J Econ Entomol 78:1154–1156Google Scholar
  8. Butler CG (1957) The control of ovary development in worker honeybees (Apis mellifera). Experientia 13:256–257Google Scholar
  9. Butler CG, Fairey EM (1963) The role of the queen in preventing oogenesis in worker honeybees. J Apic Res 2:14–18Google Scholar
  10. Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17–25Google Scholar
  11. Calderone NW, Robinson GE, Page RE (1989) Genetic structure and division of labor in honeybee societies. Experientia 45:765–767Google Scholar
  12. Contel EPB, Mestriner MA, Martins E (1977) Genetic control and developmental expression of malate dehydrogenase in Apis mellifera. Biochem Genet 15:859–876Google Scholar
  13. Crewe RM, Velthuis HHW (1980) False queens: a consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67:467–469Google Scholar
  14. Crozier RH (1979) Genetics of sociality. In: Herman HR (ed) Social insects, vol 1. Academic Press, New York, pp 223–286Google Scholar
  15. De Groot AP, Voogd S (1954) On the ovary development in queenless worker bees (Apis mellifica L.). Experientia 10:384–385Google Scholar
  16. Delaplane KS, Harbo JR (1987) Drone production by young versus old worker honeybees in queenless colonies. Apidologie 18:115–120Google Scholar
  17. Del Lama MA, Soares AEE, Mestriner MA (1985) Linkage studies in Apis mellifera using biochemical and morphological markers. J Hered 76:427–430Google Scholar
  18. Evers CA, Seeley TD (1986) Kin discrimination and aggression in honey bee colonies with laying workers. Anim Behav 34:924–944Google Scholar
  19. 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
  20. 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
  21. Frumhoff PC, Baker J (1988) A genetic component to the division of labour within honey-bee colonies. Nature 333:358–361Google Scholar
  22. Getz WM, Smith KB (1983) Genetic kin recognition: honey bees discriminate between full and half-sisters. Nature 302:147–148Google Scholar
  23. Getz WM, Smith KB (1986) Honey bee kin recognition: learning self and nestmate phenotypes. Anim Behav 34:1617–1626Google Scholar
  24. Hamilton WD (1964) The genetical theory of social behavior, I., II. J Theor Biol 7:1–16, 17–52PubMedGoogle Scholar
  25. Harbo JR (1976) The effect of insemination on the egg-laying behavior of honey bees. Ann Entomol Soc Am 69:1036–1038Google Scholar
  26. Hemmling C, Koeniger N, Ruttner F (1979) Quantitative Bestimmung der 9-oxodecensäure im Lebenszyklus der Kapbiene (Apis mellifera capensis Escholtz). Apidologie 10:227–240Google Scholar
  27. Hillesheim E, Koeniger N, Moritz R (1989) Colony performance in honeybees depends on the proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24:291–296Google Scholar
  28. Jay SC, Nelson EV (1973) The effects of laying worker honeybees (Apis mellifera L.) and their brood on the ovary development of other worker honeybees. Can J Zool 51:629–632Google Scholar
  29. Kaftanoglu O, Peng YS (1980) A washing technique for collection of honeybee semen. J Apicult Res 19:205–211Google Scholar
  30. Kerr WE, Martinho MR, Gongalves LS (1980) Kinship selection in bees. Rev Bras Genet 111:339–344Google Scholar
  31. 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 62:80–95Google Scholar
  32. Kubisová S, Haslbachová H (1978) Effects of larval extracts on the development of ovaries in caged worker honeybees. Acta Ent Bohemoslov 75:9–14Google Scholar
  33. Kubisová S, Haslbachová H, Vrkoc J (1982) Effects of fractions of larval extracts on the development of ovaries in caged worker honey bees. Acta Ent Bohemoslov 79:334–340Google Scholar
  34. Laidlaw HH (1974) Relationships of bees within a colony. Apiacta 9:49–52Google Scholar
  35. Laidlaw HH (1977) Instrumental insemination of honey bee queens. Dadant and Sons, Hamilton, IllGoogle Scholar
  36. Laidlaw HH, Page RE (1984) Polyandry in honey bees (Apis mellifera L.): sperm utilization and intracolony genetic relationships. Genetics 108:985–997Google Scholar
  37. Metcalf RA (1980) Sex ratios, parent-offspring conflict, and local competition for mates in the social wasps Polistes metricus and Polistes variatus. Am Nat 116:642–654Google Scholar
  38. Metcalf RA, Whitt GS (1977) Intra-nest relatedness in the social wasp Polistes metricus: a genetic analysis. Behav Ecol Sociobiol 2:339–351Google Scholar
  39. Moritz RFA (1983) Homogeneous mixing of honeybee semen by centrifugation. J Apic Res 24:249–255Google Scholar
  40. Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis Esch.) Behav Ecol Sociobiol 17:87–89Google Scholar
  41. Noonan KC (1986) Recognition of queen larvae by worker honey bees (Apis mellifera). Ethology 73:295–306Google Scholar
  42. Nunamaker RA, Wilson WT (1980) Some isozymes of the honey bee (Apis mellifera L.). Isozyme Bull 13:111–112Google Scholar
  43. Page RE (1986) Sperm utilization in social insects. Ann Rev Entomol 31:297–320Google Scholar
  44. 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
  45. Page RE, Erickson EH (1986) Kin recognition and virgin queen acceptance by worker honey bees (Apis mellifera L.). Anim Behav 34:1061–1069Google Scholar
  46. Page RE, Erickson EH (1988) Reproduction by worker honey bees. Behav Ecol Sociobiol 23:117–126Google Scholar
  47. Page RE, Metcalf RA (1982) Multiple mating, sperm utilization, and social evolution. Am Nat 119:263–281Google Scholar
  48. Page RE, Metcalf RA (1984) A population investment sex ratio for the honey bee (Apis mellifera L.). Am Nat 124:680–702Google Scholar
  49. Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition, and nepotism in honey-bee colonies. Nature 338:576–579Google Scholar
  50. Pellett FC (1938) History of American beekeeping. Collegiate Press, Ames, IAGoogle Scholar
  51. Perepelova L (1929) Laying workers, the ovipositing of the queens, and swarming. Bee Wld 10:69–71Google Scholar
  52. Phillips EF (1915) Beekeeping. Macmillan, New YorkGoogle Scholar
  53. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  54. Robinson GE, Page RE (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358Google Scholar
  55. Robinson GE, Page RE (1989) Genetic determination of nectar-foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol 24:317–323Google Scholar
  56. Rothenhuhler WC, Page RE (1989) Genetic variability for temporal polyethism in colonies consisting of similarly-aged worker honey bees. Apidologie 20:433–438Google Scholar
  57. Ruttner F, Koeniger N, Veith HJ (1976) Queen substance bei eierlegenden Arbeiterinnen der Honigbiene (Apis mellifera L.). Naturwissenschaften 63:434–435Google Scholar
  58. Sakagami SF (1954) Occurrence of an aggressive behavior in queenless hives, with considerations on the social organization of honeybees. Insectes Soc 1:331–343Google Scholar
  59. Sakagami SF (1958) The false-queen: fourth adjustive response in dequeened honeybee colonies. Behaviour 13:280–295Google Scholar
  60. Slessor KN, Kaminski LA, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356Google Scholar
  61. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, San FranciscoGoogle Scholar
  62. Taber S (1955) Sperm distribution in the spermathecae of multiple-mated queen honey bees. J Econ Entomol 48:522–525Google Scholar
  63. Taber S, Wendel J (1958) Concerning the number of times queen bees mate. J Econ Entomol 51:786–789Google Scholar
  64. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263Google Scholar
  65. Velthuis HHW (1976) Egg laying, aggression and dominance in bees. Proc XV Int Congr Entomol, Washington, pp 436–449Google Scholar
  66. Velthuis HHW (1985) The honeybee queen and the social organization of her colony. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Sinauer Associates, Sunderland, MAGoogle Scholar
  67. Visscher PK (1986) Kinship discrimination in queen rearing by honey bees (Apis mellifera). Behav Ecol Sociobiol 18:453–460Google Scholar
  68. Visscher PK (1989) A quantiative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254Google Scholar
  69. Voogd S (1955) Inhibition of ovary development in worker bees by extraction fluid of the queen. Experientia 11:181–182Google Scholar
  70. Voogd S (1956) The influence of a queen on the ovary development in worker bees. Experientia 12:199–201Google Scholar
  71. West-Eberhard MJ (1981) Intragroup selection and the evolution of insect societies. In: Alexander RD, Tinkle DS (eds) Natural selection and social behavior. Chiron, New York, pp 3–17Google Scholar
  72. Woyke J (1962) Natural and artificial insemination of queen honeybees. Bee Wld 43:21–25Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • Gene E. Robinson
    • 1
  • Robert E. PageJr.
    • 1
  • M. Kim Fondrk
    • 1
  1. 1.Department of EntomologyThe Ohio State UniversityColumbusUSA
  2. 2.Department of EntomologyUniversity of IllinoisUrbanaUSA
  3. 3.Department of EntomologyUniversity of CaliforniaDavisUSA

Personalised recommendations