Queens, not workers, produce the males in the stingless bee Schwarziana quadripunctata quadripunctata

Animal Behaviour

Volumn 66, Issue 2, 2003, Pages 359-368

  Tóth, Eva ^a,c   Strassmann, Joan E ^a   Imperatriz Fonseca, Vera L ^b   Queller, David C ^a  

^a RICE UNIVERSITY   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEE; QUEEN; REPRODUCTION; SOCIAL CONFLICT; WORKER CASTE;

APIDAE; APOIDEA; HYMENOPTERA; SCAPTOTRIGONA POSTICA; SCHWARZIANA; SCHWARZIANA QUADRIPUNCTATA;

EID: 0043071565     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1006/anbe.2003.2218     Document Type: Article

References (76)

1. Arévalo, E., Strassmann, J. E. & Queller, D. C. 1998. Conflicts of interests in social insects: male production in two species of Polistes. Evolution, 53, 797-805.
2. Bego, L. R. 1982. On social regulation in Nannotrigona (Scaptotrigona) postica Latreille, with special reference to male production cycles (Hym., Apidae, Meliponinae). Boletim Zoologica de Universidade de São Paulo, 7, 181-196.
3. Bego, L. R. 1990. Social regulation in Nannotrigona (Scaptotrigona) postica Lat., with special reference to productivity of colonies (Hymenoptera, Apidae, Meliponinae). Revista Brasileira Entomolica, 39, 721-739.
4. Beig, D. 1972. The production of males in queenright colonies of Trigona (Scaptotrigona) postica. Journal of Apicultural Research, 11, 33-39.
5. van Benthem, F. D. J., Imperatriz-Fonseca, V. L. & Velthuis, H. H. W. 1995. Biology of the stingless bee Plebeia remota (Holmberg): observations and evolutionary implications. Insectes Sociaux, 42, 71-87.
6. Boomsma, J. J. & Ratnieks, F. L. W. 1996. Paternity in social Hymenoptera. Proceedings of the Royal Society of London, Series B, 351, 941-975.
7. Bourke, F. G. A. 1988. Worker reproduction in the higher eusocial Hymenoptera. Quarterly Review of Biology, 63, 291-311.
8. Bourke, F. G. A. & Franks, N. R. 1995. Social Evolution in Ants. Princeton, New Jersey: Princeton University Press.
9. Bourke, F. G. A. & Ratnieks, F. L. W. 1999. Kin conflict over caste determination in social Hymenoptera. Behavioral Ecology and Sociobiology, 46, 287-297.
10. Camargo, C. A. 1972. Mating of the social bee Melipona quadrifasciata under controlled conditions (Hymenoptera, Apidae). Journal of the Kansas Entomological Society, 45, 520-523.
11. Camargo, J. M. F. 1974. Notas sobre a morfologia e biologia de Plebeia (Schwarziana) quadripunctata quadripunctata (Hymenoptera, Apidae, Meliponinae). Studia Entomologi, 17, 433-470.
12. Choe, J. C. 1988. Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Advances in Myrmecology (Ed. by J. C. Trager), pp. 163-187. Leiden: E. J. Brill.
13. Cole, B. J. 1986. The social behavior of Leptothorax allardei (Hymenoptera, Formicidae): time budgets and the evolution of worker reproduction. Behavioral Ecology and Sociobiology, 18, 165-173.
14. Contel, E. P. B. & Kerr, W. E. 1976. Origin of males in Melipona subnitida estimated from data of an isozymic polymorphic system. Genetica, 46, 271-277.
15. Crespi, B. J. 1992. Cannibalism and trophic eggs in subsocial and eusocial insects. In: Cannibalism: Ecology and Evolution Among Diverse Taxa (Ed. by M. A. Elgar & B. J. Crespi), pp. 176-213. Oxford: Oxford University Press.
16. Cunha, M. A. S., Gomes, G. M. & Oliveira Campos, L. A. 1986. Deselvolviamneto ovariano enm operarías adultas de Frieseomelita silvestri languida (Hymenoptera, Apidae) sob condiciones normais e de fandade. Ciencia e Cultura, 38, 1725-1731.
17. Drumond, P. M., Zucchi, R., Mateus, S., Bego, L. R. & Yamahe, S. 1996. Oviposition behavior of the stingless bees. XVII. Plebeia (Plebeia) droryana and ethological comparision with other Meliponinae taxa (Hymenoptera, Apidae). Japanese Journal of Entomology, 64, 385-400.
18. Drumond, P. M., Olroyd, B. P., Dollin, A. E. & Dollin, L. J. 1999. Oviposition behavior of two Australian stingless bees, Austroplebeia symei Rayment and Austroplebeia australis Friese (Hymenoptera: Apidae: Meliponini). Australian Journal of Entomology, 38, 234-241.
19. Drumond, P. M., Olroyd, B. P. & Osborne, K. 2000. Worker reproduction in Austroplebeia austrolis Friese (Hymenoptera, Apidae, Meliponini). Insectes Sociaux, 47, 333-336.
20. Engels, W. & Imperatriz-Fonseca, V. L. 1990. Caste development, reproductive strategies and control of fertility in honey bees and stingless bees. In: Social Insects: an Evolutionary Approach to Castes and Reproduction (Ed. by W. Engels), pp. 166-230. Berlin: Springer-Verlag.
21. Fletcher, D. J. C. & Ross, K. G. 1985. Regulation of reproduction in eusocial Hymenoptera. Annual Review of Entomology, 30, 319-343.
22. Foster, K. R. & Ratnieks, F. L W. 2001. The effect of sex allocation biasing on the evolution of worker policing in hymenopteran societies. American Naturalist, 158, 615-623.
23. Foster, K. R., Ratnieks, F. L. W. & Raybould, A. F. 2000. Do hornets have zombie workers? Molecular Ecology, 9, 735-742.
24. Foster, K. R., Ratnieks, F. L. W., Gyllenstrand, N. & Thorén, P. A. 2001. Colony kin structure and male production in Dolichovespula wasps. Molecular Ecology, 10, 1003-1010.
25. Goodnight, K. F. & Queller, D. C. 2000. Relatedness 5.07. http://Gsoft.smu.edu?Gsoft.html.
26. Grosso, A. F., Bego, L. R. & Martinez, A. S. 2000. The production of males in queenright colonies of Tetragonisca angustula angustula (Hymenoptera, Meliponinae). Sociobiology, 35, 475-485.
27. Hamilton, W. D. 1964. The genetical evolution of social behaviour, I, II. Journal of Theoretical Biology, 7, 1-52.
28. Hamilton, W. D. 1972. Altruism and related phenomena, mainly in social insects. Annual Review of Ecology and Systematics, 3, 193-232.
29. Hastings, M. D., Queller, D. C., Eischen, F. & Strassmann, J. E. 1998. Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Brachygastra mellifica. Behavioral Ecology, 9, 573-581.
30. Imperatriz-Fonseca, V. L. 1973. Miscellaneaous observations on the behaviour of Schwarziana quadripunctata (Hym., Apidae, Meliponinae). Boletim de Zoologia e Biologia Marina, N.S., 30, 633-640.
31. Imperatriz-Fonseca, V. L. & Zucchi, R. 1995. Virgin queens in stingless bee (Apidae, Meriponinae) colonies: a review. Apidology, 26, 231-241.
32. Inoue, T. & Roubik, D. W. 1990. Kin recognition in the stingless bee, Melipona fasciata. In: Social Insects and the Environment (Ed. by G. K. Veeresh, B. Marrik & C. A. Viraktamath), pp. 517-518. New Delhi: Oxford University Press.
33. Inoue, T., Roubik, D. W. & Suka, T. 1999. Nestmate recognition in the stingress bee Melipona panamica (Apidae, Meliponinae). Insectes Sociaux, 46, 208-218.
34. Keller, L. & Nonacs, P. 1993. The role of queen pheromones in social insects: queen control or queen signal? Animal Behaviour, 45, 787-794.
35. Kikuta, N. & Kazuki, T. 1999. Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behavioral Ecology and Sociobiology, 46, 180-189.
36. Koedam, D., Contrera, F. A. L. & Imperatriz-Fonseca, V. L. 1999. Clustered male production by workers in the stingless bee Melipona subnitida Ducke (Apidae, Meliponinae). Insectes Sociaux, 46, 387-391.
37. Machado, M. F. P. S., Contel, E. P. B. & Kerr, W. E. 1984. Proportions of males sons-of-the-queen and sons-of-workers in Plebeia droryana (Hymenoptera, Apidae) estimated from data of an MDH isozymic polymorphic system. Genetica, 65, 193-198.
38. Michener, C. D. 1974. The Social Behavior of the Bees: a Comparative Study. Cambridge, Massachusetts: Harvard University Press.
39. Moo-Valle, H., Quezada-Euán, J. J. G. & Wenseleers, T. 2001. The effect of food reserves on the production of sexual offspring in the stingless bee Melipona beecheii (Apidae, Meliponini). Insectes Socieaux, 48, 398-403.
40. Nogeira-Ferreira, F. H., Zucchi, R., da Silva-Matos, E. V. & Sakagami, S. F. 1998. Oviposition behavior of the stingless bees XXIII. Schwarziana quadripunctata with comments on the ethological diversity among representatives of the Plebeia complex (Hymenoptera, Apidae, Meliponinae). Entomological Science, 1, 511-521.
41. Oldroyd, B. P., Halling, L. A., Good, G., Wattanchaiyingcharoen, W., Barron, A. B., Nanork, P., Wongsiri, S. & Ratnieks, F. L. W. 2001. Worker policing and worker reproduction in Apis cerana. Behavioral Ecology and Sociobiology, 50, 371-377.
42. Oliveira Campos de Melo, G. A. R. 1990. Physogastric queen mating in Melipona quadrifasciata, lep. (Hymenoptera, Apidae). Revista Brasileira de Genetica, 13, 491-508.
43. Owen, R. E. & Plowright, R. C. 1982. Worker-queen conflict and male parentage in bumble bees. Behavioral Ecology and Sociobiology, 11, 94-99.
44. Peters, J. M., Queller, D. C., Imperatriz-Fonseca, V. L. & Strassmann, J. E. 1998. Microsattelite loci for stingless bees. Molecular Ecology, 7, 783-792.
45. Peters, J. M., Queller, D. C., Imperatriz-Fonseca, V. L., Roubik, D. W. & Strassmann, J. E. 1999. Mate number, kin selection, and social conflicts in stingless bees and honey bees. Proceeding of the Royal Society of London, Series B, 266, 379-384.
46. Pollock, G. B. 1996. Kin selection, kin avoidance and correlated strategies. Evolutionary Ecology, 10, 29-43.
47. Queller, D. C. 1994. A method for detecting kin discrimination within natural colonies of social insects. Animal Behaviour, 47, 569-576.
48. Queller, D. C. & Goodnight, K. F. 1989. Estimating relatedness using genetic markers. Evolution, 43, 258-275.
49. Queller, D. C. & Strassmann, J. E. 1998. Kin selection and social insects. Bioscience, 48, 165-175.
50. Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial hymenoptera. American Naturalist, 132, 217-236.
51. Ratnieks, F. L. W. & Reeve, H. K. 1992. Conflict in single-queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. Journal of Theoretical Biology, 158, 33-65.
52. Ratnieks, F. L. W. & Visscher, R. K. 1989. Worker policing in the honeybee. Nature, 342, 796-797.
53. Sakagami, S. F. 1954. Occurrence of an aggressive behavior in queenless hives, with consideration on the social organization of honeybee. Insectes Sociaux, 4, 231-243.
54. Sakagami, S. F. 1966. Techniques for the observation of behavior and social organization of stingless bees by using a special hive. Deartmento Zoologico de Secretario Agricultura de São Paulo, 19, 152-162.
55. Sakagami, S. F. 1982. Stingless bees. In: Social Insects. Vol. III (Ed. by H. R. Hermann), pp. 361-423. New York: Academic Press.
56. Sakagami, S. F. & Zucchi, R. 1963. Oviposition process in a stingless bee, Trigona (Scaptotrigona) postica Latr. (Hym.). Studia Entomologia, 6, 497-510.
57. Sakagami, S. F. & Zucchi, R. 1974. Oviposition behavior of two dwarf stingless bees, Hypotrigona (Leurotrigona) muelleri and H. (trigonisca) duckei, with notes on the temporal articulation of oviposition process in stingless bees. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology, 19, 361-420.
58. Sakagami, S. F., Beig, D., Zucchi, R. & Akahira, Y. 1963. Occurrence of ovary-developed workers in queen-right colonies of stingless bees. Revista Brasileira de Biologia, 23, 115-129.
59. Sakagami, S. F., Montenegro, M. J. & Kerr, W. E. 1965. Behavior studies of the stingless bee, with specieal reference to the oviposition process. V. Melipona quadrifasciata anthioides Lepentier. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology, 15, 578-607.
60. SAS Institute 1990. SAS/STAT User's Guide. Release 6. 4th edn. Cary, North Carolina: SAS Institute.
61. Schwarz, F. H. 1948. Stingless bees (Meriponidae) of the western hemisphere. Bulletin of the American Museum of Natural History, 90, I-XVIII, 1-546.
62. Sommeijer, M. J., Houtekamer, J. L. & Bos, W. 1984. Cell construction and egg laying in Trigona nigra var. paupera Prov. with notes on the adaptive significance of the typical behavior of stingless bees. Insectes Sociaux, 31, 199-217.
63. Starr, C. K. 1984. Sperm competition, kinship, and sociality in the aculeate Hymenoptera. In: Sperm Competition and the Evolution of Animal Mating Systems (Ed. by R. L. Smith), pp. 427-464. Orlando, Florida: Academic Press.
64. Strassmann, J. E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Sociaux, 48, 1-13.
65. Strassmann, J. E., Soils, C. R., Peters, J. M. & Queller, D. C. 1996. Strategies for finding and using polymorphic DNA microsatellite loci for studies of genetic relatedness and pedigrees. In: Molecular Zoology: Advances, Strategies and Protocols (Ed. by J. D. Ferraris & S. R. Palumbi), pp. 163-180, 528-549. New York: Wiley-Liss.
66. Suka, T. & Inoue, T. 1993. Nestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae: Meliponinae). Journal of Ethology, 11, 141-147.
67. Terada, Y. 1974. Contribuicao ao estudo da regulacao social em Leurotrigona muelleri e Frieseomlitta varia (Hymenoptera, Apidae). M.Sc. thesis, University of São Paulo.
68. Tóth, E., Queller, D. C., Imperatriz-Fonseca, V. L. & Strassmann, J. E. 2002a. Genetic and behavioral conflict over male production between workers and queens in the stingless bee Paratrigona subnuda. Behavioral Ecology and Sociobiology, 53, 1-8.
69. Tóth, E., Strassmann, J. E., Nogueira-Neto, P., Imperatriz-Fonseca, V. L. & Queller, D. C. 2002b. Male production in stingless bees: variable outcomes of queen-worker conflict. Molecular Ecology, 11, 2661-2667.
70. Trivers, R. L. & Hare, H. 1976. Haplodiploidy and the evolution of the social insects. Science, 191, 249-263.
71. Visscher, R. K. & Dukas, R. 1995. Honey bees recognize development of nesmates' ovaries. Animal Behaviour, 49, 542-544.
72. Walin, L., Sundström, L, Seppä, P. & Rosengren, R. 1998. Worker reproduction in ants: a genetic analysis. Heredity, 81, 604-612.
73. Wilson, E. O. 1971. Insect Societies. Cambridge, Massachusetts: Harvard University Press.
74. Winston, M. L. 1987. The Biology of the Honey Bee. Cambridge, Massachusetts: Harvard University Press.
75. Woyciechowski, M. & Lomnicki, A. 1987. Multiple mating of queens and the sterility of workers among eusocial hymenoptera. Journal of Theoretical Biology, 128, 317-327.
76. Zucchi, R. 1993. Ritualized dominance, evolution of queen-worker interactions and related aspects in stingless bees (Hymenoptera: Apidae). In: Evolution of Insect Societies, Comparative Sociology of Bees, Wasps and Ants (Ed. by T. Inoue & S. Yamahe), pp. 207-249. Tokyo: Hakuhinsha.