Proximate and ultimate consequences of polyandry in ants (Hymenoptera: Formicidae)

Myrmecological News

Volumn 22, Issue , 2016, Pages 1-9

  Baer, Boris ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Female choice; Genetic diversity; Kin selection; Multiple mating; Review; Social evolution; Sperm competition

Indexed keywords

EID: 84962448770     PISSN: 19944136     EISSN: 19973500     Source Type: Journal    
DOI: None     Document Type: Article

References (103)

1. ALLARD, D., BORGESEN, L., VAN HULLE, M., BOBBAERS, A., BILLEN, J. & GOBIN, B. 2006: Sperm transfer during mating in the pharaoh's ant, Monomorium pharaonis. - Physiological Entomology 31: 294-298.
2. ALLARD, D., GOBIN, B. & BILLEN, J. 2007: Timing of sperm transfer in Diacamma pallidum. - Physiological Entomology 32: 382-387.
3. ALLARD, D., GOBIN, B., ITO, F., TSUJI, K. & BILLEN, J. 2002: Sperm transfer in the Japanese queenless ant Diacamma sp. (Hymenoptera: Formicidae). - Netherlands Journal of Zoology 52: 77-86.
4. ARMITAGE, S., BOOMSMA, J. & BAER, B. 2010: Diploid male production in a leaf-cutting ant. - Ecological Entomology 35: 175-182.
5. BAER, B. 2005: Sexual selection in Apis bees. - Apidologie 36: 187-200.
6. BAER, B. 2011: The copulation biology of ants (Hymenoptera: Formicidae). - Myrmecological News 14: 55-68.
7. BAER, B. 2014: Sexual selection in social insects. In: SHUKER, D. & SIMMONS, L.W. (Eds.): The evolution of insect mating systems. - Oxford University Press, Oxford, pp. 352.
8. BAER, B. 2015: Female choice in social insects. In: PERETTI, A. & AISENBERG, A. (Eds.): Cryptic female choice in arthropods: patterns, mechanisms and prospects. - Springer, Stuttgart, pp. 461-477.
9. BAER, B., ARMITAGE, S.A.O. & BOOMSMA, J.J. 2006: Sperm storage induces an immunity cost in ants. - Nature 441: 872-875.
10. BAER, B. & BOOMSMA, J.J. 2006: Mating biology of the leafcutting ants Atta colombica and A. cephalotes. - Journal of Morphology 267: 1165-1171.
11. BAER, B., EUBEL, H., TAYLOR, N.L., O'TOOLE, N. & MILLAR, A.H. 2009a: Insights into female sperm storage from the spermathecal fluid proteome of the honeybee Apis mellifera. - Genome Biology 10: R 67.
12. BAER, B., HEAZLEWOOD, J.L., TAYLOR, N.L., EUBEL, H. & MILLAR, A.H. 2009b: The seminal fluid proteome of the honeybee Apis mellifera. - Proteomics 9: 2085-2097.
13. BAER, B. & SCHMID-HEMPEL, P. 1999: Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. - Nature 397: 151-154.
14. BAER, B. & SCHMID-HEMPEL, P. 2000: The artificial insemination of bumblebee queens. - Insectes Sociaux 47: 183-187.
15. BAER, B. & SCHMID-HEMPEL, P. 2001: Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. - Evolution 55: 1639-1643.
16. BAER, B. & SCHMID-HEMPEL, P. 2003: Bumblebee workers from different sire groups vary in susceptibility to parasite infection. - Ecology Letters 6: 106-110.
17. BAER, B. & SCHMID-HEMPEL, P. 2005: Sperm influences female hibernation success, survival and fitness in the bumblebee Bombus terrestris. - Proceedings of the Royal Society B-Biological Sciences 272: 319-323.
18. BEYE, M., HASSELMANN, M., FONDRK, M.K., PAGE, R.E. & OMHOLT, S.W. 2003: The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. - Cell 114: 419-429.
19. BIRKHEAD, T.R., HOSKEN, D.J. & PITNICK, S. 2009: Sperm biology: An evolutionary perspective. - Elsevier, Amsterdam, 642 pp.
20. BIRKHEAD, T.R. & MOLLER, A.P. 1998: Sperm competition and sexual selection.- Academic Press, New York, 650 pp.
21. BONCKAERT, W., VAN ZWEDEN, J.S., D'ETTORRE, P., BILLEN, J. & WENSELEERS, T. 2011: Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp. - Molecular Ecology 20: 3455-3468.
22. BOOMSMA, J.J. 2007: Kin selection versus sexual selection: Why the ends do not meet. - Current Biology 17: R673-R683.
23. BOOMSMA, J.J. 2009: Lifetime monogamy and the evolution of eusociality. - Philosophical Transactions of the Royal Society B-Biological Sciences 364: 3191-3207.
24. BOOMSMA, J.J. 2013: Beyond promiscuity: Mate-choice commitments in social breeding. - Philosophical Transactions of the Royal Society B-Biological Sciences 368.
25. BOOMSMA, J.J., BAER, B. & HEINZE, J. 2005: The evolution of male traits in social insects. - Annual Review of Entomology 50: 395-420.
26. BOOMSMA, J.J., BEEKMAN, M., CORNWALLIS, C.K., GRIFFIN, A.S., HOLMAN, L., HUGHES, W.O.H., KELLER, L., OLDROYD, B.P. & RATNIEKS, F.L.W. 2011: Only full-sibling families evolved eusociality. - Nature 471: E4-E5.
27. BOOMSMA, J.J. & D'ETTORRE, P. 2013: Nice to kin and nasty to non-kin: revisiting Hamilton's early insights on eusociality. - Biological Letters 9.
28. BOOMSMA, J.J. & RATNIEKS, F.L.W. 1996: Paternity in eusocial Hymenoptera. - Philosophical Transactions of the Royal Society B-Biological Sciences 351: 947-975.
29. BURNETT, W.E. & HEINZE, J. 2014: Sperm bundles in the seminal vesicles of sexually mature Lasius ant males. - Public Library of Science One 9: e93383.
30. CHAPMAN, N.C., OLDROYD, B.P. & HUGHES, W.O.H. 2007: Differential responses of honeybee (Apis mellifera) patrilines to changes in stimuli for the generalist tasks of nursing and foraging. - Behavioral Ecology and Sociobiology 61: 1185-1194.
31. COLE, B.J. 1983: Multiple mating and the evolution of social behavior in the Hymenoptera. - Behavioral Ecology and Sociobiology 12: 191-291.
32. COLE, B.J. & WIERNASZ, D.C. 1999: The selective advantage of low relatedness. - Science 285: 891-893.
33. CROZIER, R.H. & PAGE, R.E. 1985: On being the right size: Male contributions and multiple mating in social Hymenoptera. - Behavioral Ecology and Sociobiology 18: 105-116.
34. CRUDGINGTON, H.S. & SIVA-JOTHY, M.T. 2000: Genital damage, kicking and early death - The battle of the sexes takes a sinister turn in the bean weevil. - Nature 407: 855-856.
35. DE MIRANDA, J.R. & FRIES, I. 2008: Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). - Journal of Invertebrate Pathology 98: 184-189.
36. DEN BOER, S.P.A., BAER, B. & BOOMSMA, J.J. 2010: Seminal fluid mediates ejaculate competition in social insects. - Science 327: 1506-1509.
37. DEN BOER, S.P.A., BAER, B., DREIER, S., ARON, S., NASH, D.R. & BOOMSMA, J.J. 2009: Prudent sperm use by leaf-cutter ant queens. - Proceedings of the Royal Society B-Biological Sciences 276: 3945-3953.
38. DEN BOER, S.P.A., BOOMSMA, J.J. & BAER, B. 2008: Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica. - Behavioral Ecology and Sociobiology 62: 1843-1849.
39. DEN BOER, S.P.A., BOOMSMA, J.J. & BAER, B. 2013: A technique to artificially inseminate leafcutter ants. - Insectes Sociaux 60: 111-118.
40. DUVOISIN, N., BAER, B. & SCHMID-HEMPEL, P. 1999: Sperm transfer and male competition in a bumblebee. - Animal Behaviour 58: 743-749.
41. EBERHARD, W.G. 1996: Female control: Sexual selection by cryptic female choice. - Princeton University Press, Princeton, NJ, 501 pp.
42. EYER, P.A., FREYER, J. & ARON, S. 2013: Genetic polyethism in the polyandrous desert ant Cataglyphis cursor. - Behavioral Ecology 24: 144-151.
43. FJERDINGSTAD, E.J. & BOOMSMA, J.J. 1998: Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens. - Behavioral Ecology and Sociobiology 42: 257-261.
44. FOSTER, K.R. & RATNIEKS, F.L. 2000: Facultative worker policing in a wasp. - Nature 407: 692-693.
45. FRIEND, L.A. & BOURKE, A.F.G. 2012: Absence of within-colony kin discrimination in a multiple-queen ant, Leptothorax acervorum. - Ethology 118: 1182-1190.
46. GERLOFF, C.U., OTTMER, B.K. & SCHMID-HEMPEL, P. 2003: Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. - Functional Ecology 17: 582-589.
47. GERLOFF, C.U. & SCHMID-HEMPEL, P. 2005: Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). - Oikos 111: 67-80.
48. HAMILTON, W.D. 1964: The genetical evolution of social behavior I & II. - Journal of Theoretical Biology 7: (1): 1-16; (II): 17-32.
49. HEIMPEL, G.E. & DE BOER, J.G. 2008: Sex determination in the Hymenoptera. - Annual Review of Entomology 53: 209-230.
50. HERRMANN, M. & CAHAN, S.H. 2014: Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants. - Proceedings of the Royal Society B-Biological Sciences 281.
51. HIMLER, A.G., CALDERA, E.J., BAER, B.C., FERNANDEZ-MARIN, H. & MUELLER, U.G. 2009: No sex in fungus-farming ants or their crops. - Proceedings of the Royal Society B-Biological Sciences 276: 2611-2616.
52. HÖLLDOBLER, B. & WILSON, E.O. 1990: The ants. - Springer Verlag, Berlin, 732 pp.
53. HOSKEN, D.-J. & PITNICK, S. 2003: Do queens select sperm? - Trends in Ecology & Evolution 18: 107.
54. HUGHES, W.O.H. & BOOMSMA, J.J. 2005: Genetic diversity and disease resistance in leafcutting ant societies. - Evolution 58: 1251-1260.
55. HUGHES, W.O.H., OLDROYD, B.P., BEEKMAN, M. & RATNIEKS, F.L.W. 2008: Ancestral monogamy shows kin selection is key to the evolution of eusociality. - Science 320: 1213-1216.
56. HUGHES, W.O.H., SUMNER, S., VAN-BORM, S. & BOOMSMA, J.J. 2003: Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. - Proceedings of the National Academy of Sciences of the United States of America 100: 9394-9397.
57. HUNTER, F.M. & BIRKHEAD, T.R. 2002: Sperm viability and sperm competition in insects. - Current Biology 12: 121-123.
58. IZZO, A.S. & TIBBETTS, E.A. 2012: Spotting the top male: Sexually selected signals in male Polistes dominulus wasps. - Animal Behaviour 83: 839-845.
59. JAFFE, R. 2014: An updated guide to the study of polyandry in social insects. - Sociobiology 61: 1-8.
60. JAFFE, R., GARCIA-GONZALEZ, F., DEN BOER, S.P.A., SIMMONS, L.W. & BAER, B. 2012: Patterns of paternity skew among polynadrous social insects: what can they tell us about the potential for sexual selection? - Evolution 66: 3778-3788.
61. KELLER, L. & GENOUD, M. 1997: Extraordinary lifespans in ants: A test of evolutionary theories of ageing. - Nature 389: 958-960.
62. KELLER, L. & REEVE, H.K. 1994: Genetic variability, queen number, and polyandry in social Hymenoptera. - Evolution 48: 694-704.
63. KELLNER, K. & HEINZE, J. 2011: Absence of nepotism in genetically heterogeneous colonies of a clonal ant. - Ethology 117: 556-564.
64. KING, M., EUBEL, H., MILLAR, A.H. & BAER, B. 2011: Proteins within the seminal fluid are crucial to keep sperm viable in the honeybee Apis mellifera. - Journal of Insect Physiology available online.
65. KNELL, R.J. & WEBBERLEY, K.M. 2004: Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. - Biological Reviews 79: 557-581.
66. KRAUS, F.B., GERECKE, E. & MORITZ, R.F.A. 2011: Shift work has a genetic basis in honeybee pollen foragers (Apis mellifera L.). - Behavior Genetics 41: 323-328.
67. 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.). - Behavioral Ecology and Sociobiology 55: 494-501.
68. KRONAUER, D.J.C. 2009: Recent advances in army ant biology (Hymenoptera: Formicidae). - Myrmecological News 12: 51-65.
69. MATTILA, H.R. & SEELEY, T.D. 2007: Genetic diversity in honey bee colonies enhances productivity and fitness. - Science 317: 362-364.
70. MIKHEYEV, A.S. 2004: Male accessory gland size and the evolutionary transition from single to multiple mating in the fungusgardening ants. - Journal of Insect Science 4: 1-5.
71. OBERSTADT, B. & HEINZE, J. 2003: Mating biology and population structure of the ant, Leptothorax gredleri. - Insectes Sociaux 50: 340-345.
72. OLDROYD, B.P. & FEWELL, J.H. 2007: Genetic diversity promotes homeostasis in insect colonies. - Trends in Ecology & Evolution 22: 408-413.
73. OLIVEIRA, C.M., MOREIRA, J., GOMES, L.F., CAMARGO-MATHIAS, M.I. & LINO-NETO, J. 2014: Sperm bundles in the seminal vesicle of the Crematogaster victima (SMITH) adult males (Hymenoptera: Formicidae). - Neotropical Entomology 43: 201-208.
74. OPPELT, A. & HEINZE, J. 2007: Dynamics of sperm transfer in the ant Leptothorax gredleri. - Naturwissenschaften 94: 781-786.
75. PAGE, R.E. 1980: The evolution of multiple mating behavior by honey bee queens (Apis mellifera L.). - Genetics 96: 263-273.
76. PAGE, R.E. 1986: Sperm utilization in social insects. - Annual Reviews of Entomology 31: 297-320.
77. PALMER, K.A. & OLDROYD, B.P. 2003: Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): Further support for the parasite/pathogen hypothesis for the evolution of polyandry. - Naturwissenschaften 90: 265-268.
78. PAMILO, P. 1991: Life span of queens in the ant Formica exsecta. - Insectes Sociaux 38: 111-120.
79. PARKER, G.A. 1970: Sperm competition and its evolutionary consequences in the insects. - Biological Reviews 45: 525-567.
80. PEARCY, M., DELESCAILLE, N., LYBAERT, P. & ARON, S. 2014: Team swimming in ant spermatozoa. - Biology Letters 10.
81. PENG, Y., IMHOOF-BAER, B., MILLAR, A.H. & BAER, B. 2015: Consequences of Nosema apis infection for male honey bees and their fertility. - Scientific Reports 5: 10565.
82. PERRICHOT, V., LACAU, S., NERAUDEAU, D. & NEL, A. 2008: Fossil evidence for the early ant evolution. - Naturwissenschaften 95: 85-90.
83. RANGEL, J., MATTILA, H.R. & SEELEY, T.D. 2009: No intracolonial nepotism during colony fissioning in honey bees. - Proceedings of the Royal Society B-Biological Sciences 276: 3895-3900.
84. RATNIEKS, F.L.W., FOSTER, K.R. & WENSELEERS, T. 2006: Conflict resolution in insect societies. - Annual Review of Entomology 51: 581-608.
85. ROBERTS, K., EVISON, S., BAER, B. & HUGHES, W.O.H. 2015: The cost of promiscuity: sexual transmission of Nosema microsporidian parasites in polyandrous honey bees. - Scientific Reports 5: 10982, 1-7.
86. ROSS, K.G. & FLETCHER, D.J.C. 1986: Diploid male production - A significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). - Evolution 19: 283-291.
87. SCHLÜNS, H., KOENIGER, G., KOENIGER, N. & MORITZ, R.F.A. 2004: Sperm utilisation pattern in the honeybee (Apis mellifera). - Behavioral Ecology and Sociobiology 56: 458-463.
88. SCHLÜNS, H., MORITZ, R.F.A., NEUMANN, P., KRYGER, P. & KOENIGER, G. 2005: Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. - Animal Behaviour 70: 125-131.
89. SCHMID-HEMPEL, P. 1998: Parasites in social insects. - Princeton University Press, Princeton, NJ, 410 pp.
90. SHUKER, D. & SIMMONS, L.W. 2014: The evolution of insect mating systems.- Oxford University Press, Oxford, 339 pp.
91. SHYKOFF, J.A. & SCHMID-HEMPEL, P. 1991: Genetic relatedness and eusociality: Parasite-mediated selection on the genetic composition of groups. - Behavioral Ecology and Sociobiology 28: 371-376.
92. SIMMONS, L.W. 2001: Sperm competition and its evolutionary consequences in the insects.- Princeton University Press, Oxford, 434 pp.
93. SIVA-JOTHY, M.T. & STUTT, A.D. 2003: A matter of taste: direct detection of female mating status in the bedbug. - Proceedings of the Royal Society B-Biological Sciences 270: 649-652.
94. STURUP, M., BAER, B. & BOOMSMA, J.J. 2014a: Short independent lives and selection for maximal sperm survival make investment in immune defences unprofitable for leaf-cutting ant males. - Behavioral Ecology and Sociobiology 68: 947-955.
95. STURUP, M., NASH, D.R., HUGHES, W.O.H. & BOOMSMA, J.J. 2014b: Sperm mixing in the polyandrous leaf-cutting ant Acromyrmex echinatior. - Ecology and Evolution 4: 3571-3582.
96. SUNDSTRÖM, L. 1994: Sex ratio bias, relatedness asymmetry and queen mating frequency in ants. - Nature 367: 266-268.
97. TARPY, D.R. & PAGE, R.E. Jr. 2002: Sex determination and the evolution of polyandry in honey bees (Apis mellifera). - Behavioral Ecology and Sociobiology 52: 143-150.
98. TARPY, D.R. 2003: Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. - Proceedings of the Royal Society B-Biological Sciences 270: 99-103.
99. TRIVERS, R.L. & HARE, H. 1976: Haploidploidy and the evolution of the social insects. - Science 191: 249-263.
100. VISSCHER, P.K. 1998: Colony integration and reproductive conflict in honey bees. - Apidologie 29: 23-45.
101. WEBER, N.A. 1972: Gardening ants: the attines. - The American Philosophical Society, Philadelphia, PA, 146 pp.
102. YUE, C., SCHRODER, M., BIENEFELD, K. & GENERSCH, E. 2006: Detection of viral sequences in semen of honeybees (Apis mellifera): Evidence for vertical transmission of viruses through drones. - Journal of Invertebrate Pathology 92: 105-108.
103. YUE, C., SCHRODER, M., GISDER, S. & GENERSCH, E. 2007: Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). - Journal of General Virology 88: 2329-2336.