The evolution of female multiple mating in social hymenoptera

Evolution

Volumn 57, Issue 9, 2003, Pages 2067-2081

  Brown, Mark J F ^a   Schmid Hempel, Paul ^b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ETH ZURICH   (Switzerland)

Author keywords

Division of labor; Evolution of polyandry; Model; Parasites; Polyandry; Social insects

Indexed keywords

EVOLUTION; LABOR DIVISION; MULTIPLE MATING; PARASITISM; POLYANDRY; SOCIAL INSECT;

ANIMALIA; HEXAPODA; HYMENOPTERA; INSECTA;

EID: 0141427853     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00386.x     Document Type: Article

References (127)

1. Arnqvist, G., and T. Nilsson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60: 145-164.
2. Baer, B., and P. Schmid-Hempel. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151-154.
3. _. 2001. Unexpected consequences of polyandry for parasitism and fitness in the bumblebee B. terrestris. Evolution 55: 1639-1643.
4. Baer, B., E. D. Morgan, and P. Schmid-Hempel. 2001. A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. Proc. Natl. Acad. Sci. USA 98:3926-3928.
5. Banschbach, V. S., and J. M. Herbers. 1996. Complex colony structure in social insects. I. Ecological determinants and genetic consequences. Evolution 50:285-297.
6. Berkelheimer, R. C. 1984. An electrophoretic analysis of queen number in three species of dolichoderine ants. Insectes Soc. 31: 132-141.
7. Beshers, S. N., G. E. Robinson, and J. E. Mittenthal. 1999. Response thresholds and division of labor in insect colonies. Pp. 115-139 in C. Detrain, J. L. Deneubourg, and J. M. Pasteels, eds. Information processing in social insects. Birkhäuser, Basel.
8. Bonabeau, E., and G. Theraulaz. 1999. Role and variability of response thresholds in the regulation of division of labor in insect societies. Pp. 141-163 in C. Detrain, J. L. Deneubourg, and J. M. Pasteels, eds. Information processing in social insects. Birkhäuser, Basel.
9. Boomsma, J. J., and F. L. W. Ratnieks. 1996. Paternity in eusocial Hymenoptera. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351: 947-975.
10. Boomsma, J. J., and L. Sundstrom. 1998. Patterns of paternity skew in Formica ants. Behav. Ecol. Sociobiol. 42:85-92.
11. Boomsma, J. J., and T. M. Van Der Have. 1998. Queen mating and paternity variation in the ant Lasius niger. Mol. Ecol. 7: 1709-1718.
12. Boomsma, J. J., E. J. Fjerdingstad, and J. Frydenberg. 1999. Multiple paternity, relatedness and genetic diversity in Acromyrmex leaf-cutter ants. Proc. R. Soc. Lond. B Biol. Sci. 266:249-254.
13. Borgesen, L. W. 2000. Nutritional function of replete workers in the pharaoh's ant, Monomorium pharaonis (L.). Insectes Soc. 47: 141-146.
14. Brown, M. J. F., and D. M. Gordon. 1997. Individual specialisation and encounters between harvester ant colonies. Behaviour 134: 849-866.
15. Carew, M. E., W. T. Tay, and R. H. Crozier. 1997. Polygyny via unrelated queens indicated by mitochondrial DNA variations in the Australian meat ant Iridomyrmex purpureus. Insectes Soc. 44:7-14.
16. Chapuisat, M. 1998. Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. Mol. Ecol. 7:1097-1105.
17. Cole, B. J. 1983. Multiple mating and the evolution of social behavior in the Hymenoptera. Behav. Ecol. Sociobiol. 12:191-201.
18. Cole, B. J., and D. C. Wiernasz. 1999. The selective advantage of low relatedness. Science 285:891-893.
19. Corso, C. R., and A. Serzedello. 1981. A study of multiple mating habit in Atta laevigata based on the DNA content. Comp. Biochem. Physiol. B Comp. Biochem. 69:901-902.
20. Crozier, R. H., and E. J. Fjerdingstad. 2001. Polyandry in social Hymenoptera - disunity in diversity? Ann. Zool. Fenn. 38: 267-286.
21. Crozier, R. H., and R. E. Page. 1985. On being the right size: male contributions and multiple mating in social hymenoptera. Behav. Ecol. Sociobiol. 18:105-116.
22. Crozier, R. H., and P. Pamilo. 1996. Evolution of social insect colonies: sex allocation and kin selection. Oxford Univ. Press, Oxford, U.K.
23. Crozier, R. H., B. P. Oldroyd, W. T. Tay, B. E. Kaufmann, R. N. Johnson, M. E. Carew, and K. M. Jennings. 1997. Molecular advances in understanding social insect population structure. Electrophoresis 18:1672-1675.
24. Dobrzanska, J. 1959. Studies on the division of labour in ants, genus Formica. Acta Biol. Exp. 26:193-213.
25. Fjerdingstad, E. J., and J. J. Boomsma. 1998. Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens. Behav. Ecol. Sociobiol. 42:257-261.
26. Fjerdingstad, E. J., J. J. Boomsma, and P. Thorén. 1998. Multiple paternity in the leafcutter ant Atta colombica: a microsatellite DNA study. Heredity 80:118-126.
27. Foitzik, S., M. Haberl, J. Gadau, and J. Heinze. 1997. Mating frequency of Leptothorax nylanderi ant queens determined by microsatellite analysis. Insectes Soc. 44:219-227.
28. Foster, K. R., P. Seppä, F. L. W. Ratnieks, and P. A. Thorén. 1999. Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps. Behav. Ecol. Sociobiol. 46:252-257.
29. Fowler, H. G., and S. W. Robinson. 1979. Foraging by Atta sexdens (Formicidae: Attini): seasonal patterns, caste and efficiency. Ecol. Entomol. 4:239-248.
30. Franks, N. R. 1985. Reproduction, foraging efficiency and worker polymorphism in the army ant Eciton burchelli. Pp. 91-107 in M. Lindauer and B. Hölldobler, eds. Experimental behavioral ecology and sociobiology. Gustav Fischer, Stuttgart.
31. Fraser, V. S., B. Kaufmann, B. P. Oldroyd, and R. H. Crozier. 2000. Genetic influence on caste in the ant Camponotus consobrinus. Behav. Ecol. Sociobiol. 47:188-194.
32. Fuchs, S., and R. F. A. Moritz. 1998. Evolution of extreme polyandry in the honeybee Apis mellifera L. Behav. Ecol. Sociobiol. 9:269-275.
33. Fuchs, S., and V. Schade. 1994. Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155-168.
34. Gertsch, P., P. Pamilo, and S. L. Varvio. 1995. Microsatellites reveal high genetic diversity within colonies of Camponotus ants. Mol. Ecol. 4:157-260.
35. Godzinska, E. J., A. Szczuka, and J. Korczynska. 1999. Maximum longevity of workers of three ant species under laboratory conditions (Hymenoptera: Formicidae). Pol. Pismo. Entomol. 68: 47-55.
36. Gordon, D. M. 1983. Dependence of necrophoric response to oleic acid on social context in the ant, Pogonomyrmex badius. J. Chem. Ecol. 9:105-112.
37. _. 1984. Species-specific patterns in the social activities of harvester ant colonies (Pogonomyrmex). Insectes Soc. 31:74-86.
38. _. 1986. The dynamics of the daily round of the harvester ant colony (Pogonomyrmex barbatus). Anim. Behav. 34:1402-1419.
39. _. 1996. The organization of work in social insect colonies. Nature 380:121-124.
40. Haldane, J. B. S. 1949. Disease and evolution. Ricer Sci. 19(Suppl): 68-76.
41. Hamilton, W. D. 1987. Kinship, recognition, disease, and intelligence: constraints of social evolution. Pp. 81-102 in Y. Itô, J. L. Brown, and J. Kikkawa, eds. Animal societies: theory and facts. Japanese Science Society Press, Tokyo.
42. Hamilton, W. D., P. A. Henderson, and N. A. Moran. 1981. Fluctuation of environment and coevolved antagonist polymorphism as factors in the maintenance of sex. Pp. 363-382 in R. D. Alexander and D. W. Tinkle, eds. Natural selection and social behavior. Chiron Press, New York.
43. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford, U.K.
44. Hasegawa, E. 1993. Caste specialization in food storage in the dimorphic ant Colobopsis nipponicus (Wheeler). Insectes Soc. 40:261-271.
45. _. 1994. Sex allocation in the ant Colobopsis nipponicus (Wheeler). I. Population sex ratios. Evolution 48:1121-1129.
46. Heinze, J. 1998. Social and genetic structure of the ant Leptothorax risii Forel, 1892 (Insecta, Hymenoptera, Formicidae) from Gran Canada. Misc. Zool. Barc. 21:49-52.
47. Heinze, J., B. Hölldobler, and S. Trenkle. 1995a. Reproductive behavior of the ant Leptothorax (Dichothorax) pergandei. Insectes Soc. 42:309-315.
48. Heinze, J., N. Lipski, K. Schlehmeyer, and B. Hölldobler. 1995b. Colony structure and reproduction in the ant, Leptothorax acervorum. Behav. Ecol. 6:359-367.
49. Herbers, J. M. 1980. On caste ratios in ant colonies: population responses to changing environments. Evolution 34:575-585.
50. _. 1991. The population biology of Tapinoma minutum (Hymenoptera, Formicidae) in Australia. Insectes Soc. 38:195-204.
51. Herbers, J. M., and M. Cunningham. 1983. Social organization in Leptothorax longispinosus. Anim. Behav. 31:759-771.
52. Herbers, J. M., and R. L. Mouser. 1998. Microsatellite DNA markers reveal details of social structure in forest ants. Mol. Ecol. 7: 299-306.
53. Higashi, S. 1974. Worker polyethism related with body size in a polydomous red wood ant, Formica (Formica) yessensis Forel. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 19:695-705.
54. Hölldobler, B. 1976. The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behav. Ecol. Sociobiol. 1:405-423.
55. _. 1983. Territorial behavior in the green tree ant (Oecophylla smaragdina). Biotropica 15:241-250.
56. Hölldobler, B., and R. W. Taylor. 1983. A behavioral study of the primitive ant, Nothomyrmecia macrops. Insectes Soc. 30: 384-401.
57. Hölldobler, B., and E. O. Wilson. 1990. The ants. Harvard Univ. Press, Cambridge, MA.
58. Ito, M., and S. Imamura. 1974. Observations on the nuptial flight and internidal relationship in a polydomous ant, Formica (Formica) yessensis Forel. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 19:681-694.
59. Jaisson, P., D. Fresneau, R. W. Taylor, and A. Lenoir. 1992. Social organization in some primitive Australian ants. I. Nothomyrmecia macrops Clark. Insectes Soc. 39:425-438.
60. Jennions, M. D., and M. Petrie. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75:21-64.
61. Julian, G. E., and S. Cahan. 1999. Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Anim. Behav. 58:437-442.
62. Keller, L., and L. Passera. 1992. Mating system, optimal number of mating, and sperm transfer in the Argentine ant Iridomyrmex humilis. Behav. Ecol. Sociobiol. 31:359-366.
63. Keller, L., and H. K. Reeve. 1994. Genetic variability, queen number, and polyandry in social hymenoptera. Evolution 48: 694-704.
64. Keller, L., L. Sundstrom, and M. Chapuisat. 1997. Male reproductive success: paternity contribution to queens and workers in Formica ants. Behav. Ecol. Sociobiol. 41:11-15.
65. Lenoir, A. 1979. Le comportement alimentaire et la division du travail chez la fourmi Lasius niger. Bull. Biol. Fr. Belg. 113: 79-314.
66. Lenoir, A., and H. Ataya. 1983. Polyéthisme et répartition des niveaux d'activité chez la fourmi Lasius niger. Z. Tierpsychol. 62: 213-232.
67. Liersch, S., and P. Schmid-Hempel. 1998. Genetic variation within social insect colonies reduces parasite load. Proc. R. Soc. Lond. B Biol. Sci. 265:221-225.
68. MacKay, W. P. 1983. Stratification of workers in harvester ant nests (Hymenoptera: Formicidae). J. Kans. Entomol. Soc. 56:538-542.
69. Masuko, K., M. Murakami, and T. Matsumoto. 1998. Polygyny and monoandry in the ant Formica japonica (Hymenoptera: Formicidae). Zool. Sci. Tokyo 15:409-414.
70. McArthur, A. J., and M. Adams. 1996. A morphological and molecular revision of the Camponotus nigriceps group (Hymenoptera: Formicidae) from Australia. Invertebr. Taxon. 10:1-46.
71. Minkenberg, O. P. J. M., and M. Petit. 1985. Ovariole development in workers of Myrmica rubra Linnaeus (Hymenoptera, Formicidae) and its relation to age-polyethism. Ann. Soc. R. Zool. Belg. 115:29-43.
72. Mintzer, A. C. 1982. Copulatory behavior and mate selection in the harvester ant, Pogonomyrmex californicus (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 75:323-326.
73. Mirenda, J. T., and S. B. Vinson. 1981. Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim. Behav. 29:410-420.
74. Moritz, F. F. A. 1985. The effects of multiple mating on the worker-queen conflict in Apis mellifera. Behav. Ecol. Sociobiol. 16: 375-377.
75. Moritz, R. F. A., P. Kryger, G. Koeniger, N. Koeniger, A. Estoup, and S. Tingek. 1995. High degree, of polyandry in Apis dorsata queens detected by DNA microsatellite variability. Behav. Ecol. Sociobiol. 37:357-363.
76. Murakami, T., S. Higashi, and D. Windsor. 2000. Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini). Behav. Ecol. Sociobiol. 48:276-284.
77. Neumann, P., and R. F. A. Moritz. 2000. Testing genetic variance hypotheses for the evolution of polyandry in the honeybee (Apis mellifera L.). Insectes Soc. 47:271-279.
78. Page, R. E. 1980. The evolution of multiple mating behavior by honey bee queens (Apis mellifera L.). Genetics 96:263-273.
79. Page, R. E., and G. E. Robinson, 1991. The genetics of division of labour in honey bee colonies. Adv. Insect Physiol. 23:117-169.
80. Page, R. E., G. E. Robinson, N. W. Calderone, and W. C. Rothenbuhler. 1989. Genetic structure, division of labor, and the evolution of insect societies. Pp. 15-29 in M. D. Breed and R. E. Page, eds. The genetics of social evolution. Westview Press, Boulder, CO.
81. Pamilo, P. 1982. Multiple mating in Formica ants. Hereditas 97: 37-46.
82. _. 1993. Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia. Heredity 70:472-480.
83. Pamilo, P., and P. Seppa. 1994. Reproductive competition and conflicts in colonies of the ant Formica sanguinea. Anim. Behav. 48:1201-1206.
84. Pedersen, J. S., and J. J. Boomsma. 1999. Positive association of queen number and queen-mating frequency in Myrmica ants: a challenge to the genetic-variability hypotheses. Behav. Ecol. Sociobiol. 45:185-193.
85. Purvis, A., and A. Rambaut. 1995. Comparative analysis by independent contrasts (CAIC): and Apple Macintosh application for analysing comparative data. Comput. Appl. Biosci. 11:247-251.
86. Queller, D. C. 1993. Worker control of sex ratios and selection for extreme multiple mating by queens. Am. Nat. 142:346-351.
87. Ratnieks, F. L. W., and J. J. Boomsma. 1997. On the robustness of split sex ratio predictions in social Hymenoptera. J. Theor. Biol. 185:423-439.
88. Reichardt, A. K., and D. E. Wheeler. 1996. Multiple mating in the ant Acromyrmex versicolor: a case of female control. Behav. Ecol. Sociobiol. 38:219-225.
89. Retana, J., and X. Cerda. 1991. Behavioral repertoire of the ant Cataglyphis cursor (Hymenoptera, Formicidae): Is it possible to elaborate a standard specific one? J. Insect Behav. 4:139-155.
90. Robertson, H. G. 1995. Sperm transfer in the ant Carebara vidua Smith, F. (Hymenoptera, Formicidae). Insectes Soc. 42:411-418.
91. Robinson, G. E. 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37:637-665.
92. Ross, K. G., E. L. Vargo, and D. J. C. Fletcher. 1988. Colony genetic structure and queen mating frequency in fire ants of the subgenus Solenopsis (Hymenoptera: Formicidae). Biol. J. Linn. Soc. 34: 105-118.
93. Salzemann, A., and K. Jaffe. 1991. Polyethism and nest-defense in the leaf-cutting ant Atta laevigata (Smith, F.). Insectes Soc. 38: 149-159.
94. Satoh, T. 1989. Comparisons between 2 apparently distinct forms of Camponotus nawai Ito (Hymenoptera, Formicidae). Insectes Soc. 36:277-292.
95. Satoh, T., K. Masuko, and T. Matsumoto. 1997. Colony genetic structure in the mono- and polygynous sibling species of the ants Camponotus nawai and Camponotus yamaokai: DNA fingerprint analysis. Ecol. Res. 12:71-76.
96. Sauter, A., M. J. F. Brown, B. Baer, and P. Schmid-Hempel. 2001. Males of social insects can prevent queens from multiple mating. Proc. R. Soc. Lond. B Biol. Sci. 268:1449-1454.
97. Schmid-Hempel, P. 1994. Infection and colony variability in social insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346:313-321.
98. _. 1998. Parasites in social insects. Princeton Univ. Press, Princeton, NJ.
99. Schmid-Hempel, P., and R. H. Crozier. 1999. Polyandry vs. polygyny vs. parasites. Philos. Trans. R. Soc. Lond. 354:507-515.
100. Seibert, T. F., and G. O. Batzli. 1990. Honeydew resource availability, foraging strategies and fluctuations in caste size in Formica obscuripes. Bull. Ecol. Soc. Am. 71:322.
101. Seppä, P., and L. Walin. 1996. Sociogenetic organization of the red ant Myrmica rubra. Behav. Ecol. Sociobiol. 38:207-217.
102. Shattuck, S. O. 1992. Review of the dolichoderine ant genus Iridomyrmex Mayr with descriptions of three new genera (Hymenoptera: Formicidae). J. Aust. Entomol. Soc. 31:13-18.
103. Sherman, P. W., T. D. Seeley, and H. K. Reeve. 1988. Parasites, pathogens and polyandry in social Hymenoptera. Am. Nat. 131: 602-610.
104. Snyder, L. E. 1992. The genetics of social behavior in a polygynous ant. Naturwissenschaften 79:525-527.
105. Strassmann, J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc. 48:1-13.
106. Sundström, L. 1993. Genetic population structure and sociogenetic organisation in Formica truncorum (Hymenoptera; Formicidae). Behav. Ecol. Sociobiol. 33:345-354.
107. Sundström, L., and F. L. W. Ratnieks. 1998. Sex ratio conflicts, mating frequency, and queen fitness in the ant Formica truncorum. Behav. Ecol. 9:116-121.
108. Sundström, L., M. Chapuisat, and L. Keller. 1996. Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274:993-995.
109. Tarpy, D. R. 2003. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. Lond. B 270:99-103.
110. Tarpy, D. R., and R. E. Page. 2000. No behavioral control over mating frequency in queen honey bees (Apis mellifera L.): implications for the evolution of extreme polyandry. Am. Nat. 155: 820-827.
111. Traniello, J. F. A., and S. N. Beshers. 1991. Polymorphism and size-pairing in the harvester ant Pogonomyrmex badius: a test of the ecological release hypothesis. Insectes Soc. 38:121-128.
112. Tschinkel, W. R. 1987. Seasonal life history and nest architecture of a winter-active ant, Prenolepis imparts. Insectes Soc. 34: 143-164.
113. _. 1993. Resource allocation, brood production and cannibalism during colony founding in the fire ant, Solenopsis invicta. Behav. Ecol. Sociobiol. 33:209-223.
114. Villesen, P., P. J. Gertsch, J. Frydenberg, U. G. Mueller, and J. J. Boomsma. 1999. Evolutionary transition from single to multiple mating in fungus-growing ants. Mol. Ecol. 8:1819-1825.
115. Villesen, P., T. Murakami, T. R. Schultz, and J. J. Boomsma. 2002. Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. B 269: 1541-1548.
116. Ward, P. S., and R. W. Taylor. 1981. Allozyme variation, colony structure and genetic relatedness in the primitive ant Nothomyrmecia macrops (Hymenoptera: Formicidae). J. Aust. Entomol. Soc. 20:177-183.
117. Wetterer, J. K. 1990. Diel changes in forager size, activity, and load selectivity in a tropical leaf-cutting ant, Atta cephalotes. Ecol. Entomol. 15:97-104.
118. _. 1994. Ontogenetic changes in forager polymorphism and foraging ecology in the leaf-cutting ant Atta cephalotes. Oecologia 98:235-238.
119. Wetterer, J. K., D. S. Gruner, and J. E. Lopez. 1998. Foraging and nesting ecology of Acromyrmex octospinosus (Hymenoptera: Formicidae) in a Costa Rican tropical dry forest. Fla. Entomol. 81:61-67.
120. Wheeler, D. E. 1990. The development basis of worker polymorphism in fire ants. J. Insect Physiol. 36:315-321.
121. Wilson, E. O. 1975. Sociobiology: the new synthesis. Harvard Univ. Press, Cambridge, MA.
122. _. 1978. Division of labor in fire ants based on physical castes (Hymenoptera: Formicidae: Solenopsis). J. Kans. Entomol. Soc. 51:615-636.
123. _. 1980. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). I. The overall pattern in A. sexdens. Behav. Ecol. Sociobiol. 7:143-156.
124. _. 1983. Caste and division of labor in leaf-cutter ants (Hymenoptera, Formicidae, Atta). IV. Colony ontogeny of Atta cephalotes. Behav. Ecol. Sociobiol. 14:55-60.
125. Wilson, E. O., and B. Hölldobler. 1985. Caste-specific techniques of defense in the polymorphic ant Pheidole embolopyx (Hymenoptera: Formicidae). Insectes Soc. 32:3-22.
126. Woyciechowski, M. 1990. Mating behavior in the ant Myrmica rubra (Hymenoptera, Formicidae). Acta Zool. Cracov. 33:565-574.
127. Yasui, Y. 1998. The "genetic benefits" of female multiple mating reconsidered. Trends Ecol. Evol. 13:246-250.