Sexual selection in Apis bees

Apidologie

Volumn 36, Issue 2, 2005, Pages 187-200

  Baer, Boris ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Apis; Cryptic female choice; Honeybee; Polyandry; Sperm competition; Sperm storage; Sperm use

Indexed keywords

SEXUAL SELECTION;

APINAE; APIS; APIS MELLIFERA; APOIDEA; HEXAPODA; INSECTA;

EID: 22044445818     PISSN: 00448435     EISSN: None     Source Type: Journal    
DOI: 10.1051/apido:2005013     Document Type: Review

References (104)

1. Adam A. (1912) Bau und Mechanismus des Receptaculum seminis bei den Bienen, Wespen und Ameisen, Zool. Jb. Abt. Anat. Ontog. Tiere 35, 1-74.
2. Arnqvist G., Nilsson T. (2000) The evolution of polyandry: Multiple mating and female fitness in insects, Anim. Behav. 60, 145-164.
3. Baer B. (2003) Bumblebees as model organisms to study male sexual selection in social insects, Behav. Ecol. Sociobiol. 54, 521-533.
4. Baer B., Schmid-Hempel P. (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee, Nature 397, 151-154.
5. Baer B., Schmid-Hempel P. (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris, Evolution 55, 1639-1643.
6. Baer B., Schmid-Hempel P. (2003) Bumblebee workers from different sire groups vary in susceptibility to parasite infection, Ecol. Lett. 6, 106-110.
7. Baer B., Boomsma J.J. (2004) Male reproductive investment and queen mating frequency in fungus growing ants, Behav. Ecol. 15, 426-432.
8. Baer B., Schmid-Hempel P. (2005) Sperm influences female hibernation success, survival and fitness in the bumblebee Bambus terrestris, Proc. R. Soc. Lond. 272, 319-329.
9. Baer B., Maile R., Schmid-Hempel P., Morgan E.D., Jones G.R. (2000) Chemistry of a mating plug in bumblebees, J. Chem. Ecol. 26, 1869-1875.
10. Baer B., Morgan E.D., Schmid-Hempel P. (2001) A non-specific fatty acid within the bumblebee mating plug prevents females from remating, Proc. Natl. Acad. Sci. USA 98, 3926-3928.
11. Baer B., Schmid-Hempel P., Hoeg J.T., Boomsma J.J. (2003) Sperm length, sperm storage and mating system characteristics in bumblebees, Insectes Soc. 50, 101-108.
12. Baudry E., Solignac M., Garnery L., Gries M., Cornuet J.M., Koeniger N. (1998) Relatedness among honeybees (Apis mellifera) of a drone congregation, Proc. R. Soc. Lond. B 26, 2009-2014.
13. Berg S., Koeniger N., Koeniger G., Fuchs S. (1997) Body size and reproductive success of drones (Apis mellifera L.), Apidologie 28, 449-460.
14. Birkhead T.R., Moller A.P. (1998) Sperm competition and sexual selection, Academic Press, New York.
15. Boomsma J.J., Ratnieks F.L.W. (1996) Paternity in eusocial Hymenoptera, Phil. Trans. R. Soc. Lond. B 351, 947-975.
16. Boomsma J.J., Baer B., Heinze J. (2005) The evolution of male traits in social insects, Annu. Rev. Entomol. 50, 395-420.
17. Bozina K.D. (1961) How long does the queen live? Pchelovodstvo 38, 13 (in Russian).
18. Bresslau E. (1905) Der Samenblasengang der Bienenkönigin, Zool. Anz. 29, 299-325.
19. Briskie J.V., Montgomerie R. (1992) Sperm size and sperm competition in birds, Proc. R. Soc. Lond. B 247, 89-95.
20. Brown M.J.F., Baer B. (2005) The evolutionary significance of long copulation duration in bumble bees, Apidologie 36, 157-167.
21. Crozier R.H., Page R.E. (1985) On being the right size: Male contributions and multiple mating in social hymenoptera, Behav. Ecol. Sociobiol. 18, 105-116.
22. Crazier R.H., Pamilo P. (1996) Evolution of social insect colonies, University Press, Oxford.
23. Crozier R.H., Fjerdingstad E.J. (2001) Polyandry in social hymenoptera: Disunity in diversity? Ann. Zool. Fenn. 38, 267-285.
24. Denny A.J., Franks N.R., Powell S., Edwards K.J. (2004) Exceptionally high levels of multiple mating in an army ant, Naturwissenschaften 91, 396-399.
25. Duvoisin N., Baer B., Schmid-Hempel P. (1999) Sperm transfer and male competition in a bumblebee, Anim. Behav. 58, 743-749.
26. Eberhard W.G. (1996) Female control: Sexual selection by cryptic female choice, Princeton University Press, Princeton, New Jersey.
27. Eberhard W.G., Cordero C. (1995) Sexual selection by cryptic female choice on male seminal products. A new bridge between sexual selection and reproductive physiology, Trends Ecol. Evol. 10, 493-496.
28. Eickwort G.C., Ginsberg H.S. (1980) Foraging and mating behavior in Apoidea, Annu. Rev. Entomol. 25, 421-446.
29. Foitzik S., Heinze J., Oberstadt B., Herbers J.M. (2002) Mate guarding and alternative reproductive tactics in the ant Hypoponera opacior, Anim. Behav. 63, 597-604.
30. Franck P., Coussy H., Le Conte Y., Solignac M., Garnery L., Cornuet J.M. (1999) Microsatellite analysis of sperm admixture in honeybee, Insect Mol. Biol. 8, 419-421.
31. Franck P., Solignac M., Vautrin D., Cornuet J.M., Koeniger G., Koeniger N. (2002) Sperm competition and last-male precedence in the honeybee, Anim. Behav. 64, 503-509.
32. Fuchs S., Moritz R.F.A. (1999) Evolution of extreme polyandry in the honeybee Apis mellifera, Behav. Ecol. Sociobiol. 45, 269-275.
33. Gage M.J.G. (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies, Proc. R. Soc. Lond. B 258, 247-254.
34. Gomendio M., Roldan E.R.S. (1991) Sperm competition influences sperm size in mammals, Proc. R. Soc. Lond. B 243, 181-186.
35. Gries M., Koeniger N. (1996) Straight forward to the queen: Pursuing honeybee drones (Apis mellifera) adjust their body axis to the direction of the queen, J. Comp. Physiol. A 179, 539-544.
36. Haberl M., Tautz D. (1998) Sperm usage in honey bees, Behav. Ecol. Sociobiol. 42, 247-255.
37. Hamilton W.D. (1964) The genetical evolution of social behavior, J. Theor. Biol. 7, 1-16; 17-32.
38. Harbo J.R. (1979) The rate of depletion of spermatozoa in the queen honey bee Apis mellifera spermatheca, J. Apic. Res. 18, 3.
39. Harbo J.R. (1990) Artificial mixing of spermatozoa from honeybees and evidence for sperm competition, J. Apic. Res. 29, 151-158.
40. Hölldobler B., Bartz S.H. (1985) Sociobiology of reproduction in ants, in: Hölldobler B., Lindauer M. (Eds.), Experimental Behavioural Ecology and Sociobiology, Gustav Fischer Verlag, Stuttgart, New York, pp. 237-257.
41. Hölldobler B., Wilson E.O. (1990) The Ants, Springer Verlag, Berlin.
42. Hosken D.J. (1997) Sperm competition in bats, Proc. R. Soc. Lond. B 264, 385-392.
43. Jennions M.D., Petrie M. (2000) Why do females mate multiply? A review of the genetic benefits, Biol. Rev. 75, 21-64.
44. Jones J.C., Myerscough M.R., Graham S., Oldroyd B.P. (2004) Honey bee nest thermoregulation: Diversity promotes stability, Science 305, 402-404.
45. Kerr W.E., Bueno D. (1970) Natural crossing between Apis mellifera adansonii and Apis mellifera ligustica, Evolution 24, 145-148.
46. Koeniger G. (1990) The role of the mating sign in honey bees, Apis mellifera L.: Does it hinder or promote multiple mating? Anim. Behav. 39, 444-449.
47. Koeniger N., Koeniger G. (1991) An evolutionary approach to mating behaviour and drone copulatory organs in Apis, Apidologie 22, 581-590.
48. Koeniger N., Koeniger G. (2000) Reproductive isolation among species of the genus Apis, Apidologie 31, 313-339.
49. Koeniger G., Koeniger N., Fabritius M. (1979) Some detailed observations of mating in the honeybee, Bee World 60, 53-57.
50. Koeniger G., Koeniger N., Pechhacker H., Ruttner F., Berg S. (1989a) Assortative mating in a mixed population of European honeybees Apis mellifera ligustica and Apis mellifera carnica, Insectes Soc. 36, 129-138.
51. Koeniger N., Koeniger G., Wongsiri S. (1989b) Mating and sperm transfer in Apis florea, Apidologie 20, 413-418.
52. Koeniger G., Koeniger N., Tingek S. (1996) A scientific note on weight and sperm numbers of drones of Apis nuluensis, Apidologie 27, 427-428.
53. Koeniger G., Koeniger N., Tingek S., Kelitu A. (2000) Mating flights and sperm transfer in the dwarf honeybee Apis andreniformis (Smith, 1858), Apidologie 31, 301-311.
54. Koeniger G., Koeniger N., Tingek S., Phiancharoen M. (2005) Variance in spermatozoa number among Apis dorsata drones and among Apis mellifera drones, Apidologie 36, 279-284.
55. Kraus F.B., Neumann P., van Praagh J., Moritz R.F.A. (2004) Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.), Behav. Ecol. Sociobiol. 55, 494-501.
56. Kronauer D.J., Schöning C., Pedersen J.S., Boomsma J.J., Gadau J. (2004) Extreme queen-mating frequency and colony fission in African army ants, Mol. Ecol. 13, 2381-2388.
57. Laidlaw H.H., Page R.E. (1984) Polyandry in honeybees Apis mellifera sperm utilization and intracolony genetic relationships, Genetics 108, 985-998.
58. Lee P.C. (1985) Reproduction and growth of temperate-evolved honey bee colonies (Apis mellifera L.), M. Sc. thesis, Simon Fraser University, Burnaby, B.C.
59. Lee P.C., Winston M.L. (1985) The effect of swarm size and date of issue on comb construction in newly founded colonies of honeybees Apis mellifera, Can. J. Zool. 63, 524-527.
60. Lino Neto J., Dolder H. (2002) Sperm structure and ultrastructure of the fire ant Solenopsis invicta (Buren) (Hymenoptera, Formicidae), Tissue and Cell 34, 124-128.
61. Moritz R.F.A. (1986) Intracolonial worker relationship and sperm competition in the honeybee Apis mellifera, Experientia 42, 445-448.
62. Morrow E.H., Gage M.J.G. (2000) The evolution of sperm length in moths, Proc. R. Soc. Lond. B 267, 307-313.
63. Oldroyd B.P., Smolenski A.J., Cornuet J.M., Wongsiri S., Estoup A., Rinderer T.E., Crozier R.H. (1995) Levels of polyandry and intracolonial genetic relationships in Apis florea, Behav. Ecol. Sociobiol. 37, 329-335.
64. Oldroyd B.P., Smolenski A.J., Cornuet J.M., Wongsiri S., Estoup A., Rinderer T.E., Crozier R.H. (1996) Levels of polyandry and intracolonial genetic relationships in Apis dorsata (Hymenoptera: Apidae), Ann. Entomol. Soc. Am. 89, 276-283.
65. Oldroyd B.P., Clifton M.J., Wongsiri S., Rinderer T.E., Sylvester H.A., Crozier R.H. (1997) Polyandry in the genus Apis, particularly Apis andreniformis, Behav. Ecol. Sociobiol. 40, 17-26.
66. Oldroyd B.P., Clifton M.J., Parker K., Wongsiri S., Rinderer T.E., Crozier R.H. (1998) Evolution of mating behaviour in the genus Apis and an estimate of mating frequency in Apis cerana (Hymenoptera: Apidae), Ann. Entomol. Soc. Am. 91, 700-709.
67. Page R.E. (1986) Sperm utilization in social insects, Annu. Rev. Entomol. 31, 297-320.
68. Page R.E., Metcalf R.A. (1982) Multiple mating, sperm utilization and social evolution, Am. Nat. 119, 263-282.
69. Page R.E., Metcalf R.A. (1984) A population investment sex ratio for the honeybee Apis mellifera, Am. Nat. 124, 680-702.
70. Pamilo P. (1991) Life span of queens in the ant Formica exsecta, Insectes Soc. 38, 111-120.
71. Parker G.A. (1970) Sperm competition and its evolutionary consequences in the insects, Biol. Rev. 45, 525-567.
72. Pflugfelder J., Koeniger N. (2003) Fight between virgin queens (Apis mellifera) is initiated by contact to the dorsal abdominal surface, Apidologie 34, 249-256.
73. Radloff S.E., Hepburn H.R., Koeniger G. (2003) Comparison of flight design of asian honeybee drones, Apidologie 34, 1-6.
74. Raignier A., van Boven J.K.A. (1955) Étude taxonomique, biologique et biométrique des Dorylus du sous genre Anomma (Hymenoptera, Formicidae), Ann. Mus. R. Congo Belg. 2, 1-359.
75. Ratnieks F.L.W., Boomsma J.J. (1995) Facultative sex allocation by workers and the evolution of polyandry by queens in social Hymenoptera, Am. Nat. 145, 969-993.
76. Rheindt F.E., Gadau J., Strehl C.P., Hölldobler B. (2004) Extremely high mating frequency in the Florida harvester ant (Pogonomyrmex badius), Behav. Ecol. Sociobiol. 56, 472-481.
77. Ruttner F. (1954) Mehrfache Begattung der Bienenkönigin, Zool. Anz. 153, 99-105.
78. Ruttner F. (1956) The mating of the honey bee, Bee World 3, 2-15.
79. Ruttner F. (1975) Die instrumentelle Besamung der Bienenkönigin, 2nd ed., Apimondia, Bukarest.
80. Ruttner F. (1985) Reproductive behaviour in honeybees, in: Hölldobler B., Lindauer M. (Eds.), Experimental Behavioural Ecology and Sociobiology, Gustav Fischer Verlag, Stuttgart, Fortschr. Zool. 31, 225-236.
81. Ruttner F. (1988) Biogeography and taxonomy of honeybees, Springer, Berlin, 284 p.
82. Ruttner F., Koeniger G. (1971) The filling of the spermatheca of the honey bee queen: active migration or passive transport of the spermatozoa, Z. Vgl. Physiol. 72, 411-422.
83. Ruttner H., Ruttner F. (1972) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen, V. Drohnensammelplätze und Paarungsdistanz, Apidologie 3, 203-232.
84. Sauter A., Brown M.J.F., Baer B., Schmid-Hempel P. (2001) Males of social insects can prevent queens from multiple mating, Proc. R. Soc. Lond. B 268, 1449-1454.
85. Schlüns H., Koeniger G., Koeniger N., Moritz R.F.A. (2004) Sperm utilisation pattern in the honeybee (Apis mellifera), Behav. Ecol. Sociobiol. 56, 458-463.
86. Schlüns H., Moritz R.F.A., Lattorff H.M.G., Koeniger G. (2005) Paternity skew in seven species of honeybees (Hymenoptera: Apidae: Apis), Apidologie 36, 201-209.
87. Seeley T.D., Visscher P.K. (1985) Survival of honeybees Apis mellifera in cold climates: The critical timing of colony growth and reproduction, Ecol. Entomol. 10, 81-88.
88. Shykoff J.A., Schmid-Hempel P. (1991) Parasites and the advantage of genetic variability within social insect colonies, Proc. R. Soc. Lond. B 243, 55-58.
89. Simmons L.W. (2001) Sperm competition and its evolutionary consequences in the insects, Princeton University Press, Oxford.
90. Snodgrass R.E. (1984) Anatomy of the honeybee, Comstock Publishing Associates, Ithaca.
91. Stockley P. (1997) Sexual conflict resulting from adaptations to sperm competition, Trends Ecol. Evol. 12, 154-159.
92. Strassmann J. (2001) The rarity of multiple mating by females in the social Hymenoptera, Insectes Soc. 48, 1-13.
93. Takahashi J.I., Nakamura J. (2003) A scientific note on levels of polyandry of 2 queens of the Himalayan giant honeybee, Apis laboriosa, Apidologie 34, 191-192.
94. Tarpy D.R. (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth, Proc. R. Soc. Lond. B 270, 99-103.
95. Tarpy D.R., Page R.E. (2002) Sex determination and the evolution of polyandry in honey bees (Apis mellifera), Behav. Ecol. Sociobiol. 52, 143-150.
96. Tarpy D.R., Nielsen R., Nielsen D.I. (2004) A scientific note on the revised estimates of effective paternity frequency in Apis, Insectes Soc. 51, 203-204.
97. Trivers R.L., Hare H. (1976) Haplodiploidy and the evolution of the social insects, Science 191, 249-263.
98. Weber N.A. (1972) Gardening ants: The attines, The American Philosophical Society, Philadelphia.
99. Winston M.L. (1991) The biology of the honey bee, Harvard University Press, Cambridge, Massachusetts, London.
100. Woyciechowski M., Kabat L., Krol E. (1994) The function of the mating sign in honey bees, Apis mellifera L.: New evidence, Anim. Behav. 47, 733-735.
101. Woyke J. (1964) Causes of repeated mating flights by queen honeybees, J. Apic. Res. 3, 17-23.
102. Woyke J. (1983) Dynamics of entry of spermatozoa into the spermatheca of instrumentally inseminated queen honey bees Apis mellifera, J. Apic. Res. 22, 150-154.
103. Yu R., Omholt S.W. (1999) Early developmental processes in the fertilised honeybee (Apis mellifera) oocyte, J. Insect Physiol. 45, 763-767.
104. Zander E. (1922) Der Bau der Biene, Eugen Ulmer Verlag, Stuttgart, 182 p.