, Volume 91, Issue 6, pp 291–304 | Cite as

Multilevel selection and social evolution of insect societies

  • Judith Korb
  • Jürgen Heinze


How sterile, altruistic worker castes have evolved in social insects and how they are maintained have long been central topics in evolutionary biology. With the advance of kin selection theory, insect societies, in particular those of haplodiploid bees, ants, and wasps, have become highly suitable model systems for investigating the details of social evolution and recently also how within-group conflicts are resolved. Because insect societies typically do not consist of clones, conflicts among nestmates arise, for example about the partitioning of reproduction and the allocation of resources towards male and female sexuals. Variation in relatedness among group members therefore appears to have a profound influence on the social structure of groups. However, insect societies appear to be remarkably robust against such variation: division of labor and task allocation are often organized in more or less the same way in societies with high as in those with very low nestmate relatedness. To explain the discrepancy between predictions from kin structure and empirical data, it was suggested that constraints—such as the lack of power or information—prevent individuals from pursuing their own selfish interests. Applying a multilevel selection approach shows that these constraints are in fact group-level adaptation preventing or resolving intracolonial conflict. The mechanisms of conflict resolution in insect societies are similar to those at other levels in the biological hierarchy (e.g., in the genome or multicellular organisms): alignment of interests, fair lottery, and social control. Insect societies can thus be regarded as a level of selection with novelties that provide benefits beyond the scope of a solitary life. Therefore, relatedness is less important for the maintenance of insect societies, although it played a fundamental role in their evolution.


Social Insect Inclusive Fitness Insect Society Multilevel Selection Relatedness Asymmetry 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Our studies were supported by DFG (HE-1623/15 and KO-1895/2). We thank three referees for their valuable comments on a first draft of our manuscript. This paper is dedicated to Ernst Mayr, with our best wishes for his 100th birthday.


  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237Google Scholar
  3. Anderson C, Ratnieks FLW (1999) Task partitioning in insect societies. I. Effect of colony size on queuing delay and colony ergonomic efficiency. Am Nat 154:521–535PubMedGoogle Scholar
  4. Aoki S (1987) Evolution of sterile soldiers in aphids. In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Scientific Societies, Tokyo, pp 53–65Google Scholar
  5. Atlan A, Mercot H, Landre C, Montchamp-Moreau C (1997) The sex-ratio trait in Drosophila simulans: geographical distribution of distortion and resistance. Evolution 51:1886–1895Google Scholar
  6. Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite load and fitness in a bumble-bee. Nature 397:151–153Google Scholar
  7. Banschbach VA, Herbers JM (1996) Complex colony structure in social insects. II. Reproduction, queen-worker conflict, and levels of selection. Evolution 50:298–307Google Scholar
  8. Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci USA 76:5764–5768Google Scholar
  9. Beekman M, Sumpter DJT, Ratnieks FLW (2001) Phase transition between disordered and ordered foraging in Pharaoh’s ants. Proc Natl Acad Sci USA 98:9703–9706CrossRefPubMedGoogle Scholar
  10. Beekman M, Komdeur J, Ratnieks FLW (2003) Reproductive conflicts in social animals: who has power? Trends Ecol Evol 188:277–282CrossRefGoogle Scholar
  11. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440PubMedGoogle Scholar
  12. Bonabeau E, Theraulaz G, Deneubourg JL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 12:188–193CrossRefGoogle Scholar
  13. Boomsma JJ, Grafen A (1990) Intraspecific variation in ant sex ratios and the Trivers–Hare hypothesis. Evolution 44:1026–1034Google Scholar
  14. Boomsma JJ, Grafen A (1991) Colony-level sex ratio selection in the eusocial Hymenoptera. J Evol Biol 3:383–407Google Scholar
  15. Boomsma JJ, Ratnieks FLW (1996) Paternity in social Hymenoptera. Philos Trans R Soc Lond B 351:947–975Google Scholar
  16. Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311CrossRefGoogle Scholar
  17. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257CrossRefGoogle Scholar
  18. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.Google Scholar
  19. Braude S (2000) Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating. Behav Ecol 11:7–12CrossRefGoogle Scholar
  20. Brown WD, Keller L (2000) Colony sex ratios vary with queen number but not relatedness asymmetry in the ant Formica exsecta. Proc R Soc Lond B 267:1751–1757PubMedGoogle Scholar
  21. Brown WD, Keller L, Sundström L (2002) Sex allocation in mound-building ants: the roles of resources and queen replenishment. Ecology 83:1945–1952Google Scholar
  22. Buss L (1987) The evolution of individuality. Princeton University Press, Princeton, N.J.Google Scholar
  23. Camazine S, Deneubourg JL, Franks N, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton, N.J.Google Scholar
  24. Chan GL, Hingle A, Bourke AFG (1999) Sex allocation in a facultatively polygynous ant: between-population and between-colony variation. Behav Ecol 10:409–421CrossRefGoogle Scholar
  25. Chapman TW, Crespi BJ, Kranz BD, Schwarz MP (2000) High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips. Proc Natl Acad Sci USA 97:1648–1650CrossRefPubMedGoogle Scholar
  26. Choe JC (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. Brill, Leiden, pp 163–187Google Scholar
  27. Cockburn A (1998) Evolution of helping behaviour in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177Google Scholar
  28. Coenen-Stass D, Schaarschmidt B, Lamprecht I (1980) Temperature distribution and calorimetric determination of heat production in the nest of the wood ant, Formica polyctena (Hymenoptera, Formicidae). Ecology 61:238–244Google Scholar
  29. Crozier RH, Fjerdingstad EJ (2001) Polyandry in social Hymenoptera: disunity in diversity? Ann Zool Fenn 38:267–285Google Scholar
  30. Crozier RH, Luykx P (1985) The evolution of termite eusociality is unlikely to have been based on a male-haploid analogy. Am Nat 126:867–869CrossRefGoogle Scholar
  31. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  32. Cuvillier-Hot V, Gadagkar R, Peeters C, Cobb M (2002) Regulation of reproduction in a queenless ant: aggression, pheromones and reduction in conflict. Proc R Soc Lond B 269:1295–1300CrossRefPubMedGoogle Scholar
  33. Darwin C (1859) On the origin of species by means of natural selection. John Murray, LondonGoogle Scholar
  34. Darwin C (1871) The descent of man and selection in relation to sex. Appleton, New YorkGoogle Scholar
  35. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  36. Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (Ed) Social insects, II. Academic Press, New York, pp 1–76Google Scholar
  37. Dugatkin LA, Reeve HK (1994) Behavioral ecology and levels of selection: dissolving the group selection controversy. Adv Stud Behav 23:101–133Google Scholar
  38. Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology, 4th edn. Blackwell Science, Oxford, pp 228–253Google Scholar
  39. Fisher RA (1930) The genetical theory of natural selection. Clarendon, OxfordGoogle Scholar
  40. Fjerdingstad EJ (2004) Multiple paternity and colony homeostasis in Lasius niger ants. Behav Ecol Sociobiol 55:  10.1007/s00265-004-0759-8 Google Scholar
  41. Fjerdingstad EJ, Gertsch PJ, Keller L (2002) Why do some social insect queens mate with several males? Testing the sex-ratio manipulation hypothesis in Lasius niger. Evolution 56:553–562PubMedGoogle Scholar
  42. Foitzik S, Heinze J (2000) Intraspecific parasitism and split sex ratios in a monogynous, monandrous ant (Leptothorax nylanderi). Behav Ecol Sociobiol 47:424–431CrossRefGoogle Scholar
  43. Foitzik S, Herbers JM (2001) Colony structure of a slavemaking ant. I. Intracolony relatedness, worker reproduction, and polydomy. Evolution 55:307–315PubMedGoogle Scholar
  44. Foitzik S, Strätz M, Heinze J (2003) Ecology, life history, and resource allocation in the ant, Leptothorax nylanderi. J Evol Biol 16:670–680CrossRefGoogle Scholar
  45. Foster KR, Gulliver J, Ratnieks FLW (2002) Why workers do not reproduce: worker policing in the European hornet Vespa crabro. Insectes Soc 49:41–44CrossRefGoogle Scholar
  46. Fournier D, Keller L, Passera L, Aron S (2003) Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula. Evolution 57:1336–1342PubMedGoogle Scholar
  47. Frank SA (1985) Hierarchical selection theory and sex ratio. II. On applying the theory, and a test with fig wasps. Evolution 39:949–964Google Scholar
  48. Frank SA (1990) Sex allocation theory for birds and mammals. Annu Rev Ecol Syst 21:13–55CrossRefGoogle Scholar
  49. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78PubMedGoogle Scholar
  50. Frank SA (1997) Foundations of social evolution. Princeton University Press, Princeton, N.J.Google Scholar
  51. Franks NR, Pratt SC, Mallon EB, Britton NF, Sumpter DJT (2002) Information flow, opinion polling and collective intelligence in house-hunting social insects. Philos Trans R Soc Lond B 357:1567–1583CrossRefGoogle Scholar
  52. Frumhoff PC, Baker J (1988) A genetic component to the division of labour within honey bee colonies. Nature 333:358–361CrossRefGoogle Scholar
  53. Fuchs S, Schade V (1994) Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155–168Google Scholar
  54. Gadagkar R (1985) Evolution of insect sociality: a review of some attempts to test modern theories. Proc Indian Acad Sci (Anim Sci) 94:309–324Google Scholar
  55. Gadagkar R (1990) Evolution of eusociality: the advantage of assured fitness returns. Philos Trans R Soc Lond B 329:17–25Google Scholar
  56. Gadau J, Strehl C-P, Oettler J, Hölldobler B (2003) Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids. Mol Ecol 12:1931–1938CrossRefPubMedGoogle Scholar
  57. Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079PubMedGoogle Scholar
  58. Goodnight CJ, Stevens L (1997) Experimental studies of group selection: what do they tell us about group selection in nature? Am Nat 150:S59–S79CrossRefGoogle Scholar
  59. Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124Google Scholar
  60. Grafen A (1984) Natural selection, kin selection and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology, 2nd edn. Blackwell Science, Oxford, pp 62–84Google Scholar
  61. Greeff J (1996) Effects of thelytokous worker reproduction in kin selection and conflict in the Cape honeybee, Apis mellifera capensis. Philos Trans R Soc Lond B 351:617–625Google Scholar
  62. Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636CrossRefPubMedGoogle Scholar
  63. Haldane JBS (1932) The causes of evolution. Longmans Green, LondonGoogle Scholar
  64. Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 97:354–356CrossRefGoogle Scholar
  65. Hamilton WD (1964) The genetical evolution of social behaviour. I, II. J Theor Biol 7:1–52PubMedGoogle Scholar
  66. Hamilton WD (1970) Selfish and spiteful behaviour in an evolutionary model. Nature 228:1218–1220PubMedGoogle Scholar
  67. Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232CrossRefGoogle Scholar
  68. Hamilton WD (1975) Innate social aptitudes in man: an approach from evolutionary genetics. In: Fox R (ed) Biosocial anthropology. Malaby, London, pp 133–155Google Scholar
  69. Hammond RL, Bruford MW, Bourke AFG (2002) Ant workers selfishly bias sex ratios by manipulating female development. Proc R Soc Lond B 269:173–178CrossRefGoogle Scholar
  70. Hammond RL, Bruford MW, Bourke AFG (2003) Male parentage does not vary with colony kin structure in a multiple-queen ant. J Evol Biol 16:446–455PubMedGoogle Scholar
  71. Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–2429PubMedGoogle Scholar
  72. Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci USA 100:12836–12840CrossRefPubMedGoogle Scholar
  73. Heinrich B (1993) The hot-blooded insect. Harvard University Press, Cambridge, Mass.Google Scholar
  74. Heinze J (1995) Reproductive skew and relatedness in Leptothorax ants. Proc R Soc Lond B 261:375–379Google Scholar
  75. Heinze J (1996) The reproductive potential of workers in slave-making ants. Insectes Soc 43:319–328Google Scholar
  76. Heinze J, Hölldobler B (1995) Thelytokous parthenogenesis and dominance hierarchies in the ponerine ant, Platythyrea punctata (F. Smith). Naturwissenschaften 82:40–41CrossRefGoogle Scholar
  77. Heinze J, Cover SP, Hölldobler B (1995) Neither worker nor queen: an ant caste specialized on the production of male eggs. Psyche 102:173–185Google Scholar
  78. Heinze J, Strätz M, Pedersen JS, Haberl M (2000) Microsatellite analysis suggests occasional worker reproduction in the monogynous ant Crematogaster smithi. Insectes Soc 47:299–301Google Scholar
  79. Helms KR (1999) Colony sex ratios, conflict between queens and workers, and apparent queen control in the ant Pheidole desertorum. Evolution 53:1470–1478Google Scholar
  80. Henderson G (1998) Primer pheromones and possible soldier caste influence on the evolution of sociality in lower termites. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview, Boulder, Colo., pp 314–330Google Scholar
  81. Herbers JM (1982) Queen-number and colony ergonomics in Leptothorax longispinosus. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview, Boulder, Colo., pp 238–242Google Scholar
  82. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, Mass.Google Scholar
  83. Horstmann K (1983) Regulation der Temperatur in Waldameisennestern (Formica polyctena Förster). Z Naturforsch 38:508–510Google Scholar
  84. Horstmann K (1990) Zur Entstehung des Wärmezentrums in Waldameisennestern (Formica polyctena Förster; Hymenoptera, Formicidae). Zool Beitr NF 33:105–124Google Scholar
  85. Iwanishi S, Hasegawa E, Ohkawara K (2003) Worker oviposition and policing behaviour in the myrmicine ant Aphaenogaster smythiesi japonica Forel. Anim Behav 66:513–519CrossRefGoogle Scholar
  86. Jeanne R (1975) The adaptiveness of social wasp nest architecture. Q Rev Biol 50:267–287CrossRefGoogle Scholar
  87. Jeon J, Choe JC (2003) Reproductive skew and the origin of sterile castes. Am Nat 161:206–224CrossRefPubMedGoogle Scholar
  88. Karsai I, Wenzel JW (1998) Productivity, individual-level and colony-level flexibility, and organization of work as consequences of colony size. Proc Natl Acad Sci USA 96:8665–8669CrossRefGoogle Scholar
  89. Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 146:610–632CrossRefGoogle Scholar
  90. Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Evol Ecol 10:355–360CrossRefGoogle Scholar
  91. Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. Trend Ecol Evol 12:99–103CrossRefGoogle Scholar
  92. Keller L, Nonacs P (1993) The role of queen pheromones in social insects; queen control or queen signal? Anim Behav 45:787–794Google Scholar
  93. Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704Google Scholar
  94. Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291–315Google Scholar
  95. Keller L, Reeve HK (1999) Dynamics of conflicts within insect societies. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 153–175Google Scholar
  96. Korb J (2003) Thermoregulation and ventilation of termite mounds. Naturwissenschaften 90:212–219PubMedGoogle Scholar
  97. Korb J, Linsenmair KE (2000) Ventilation of termite mounds: new results require a new model. Behav Ecol 11:486–494CrossRefGoogle Scholar
  98. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  99. Krieger MJB, Keller L (2000) Mating frequency and genetic structure of the Argentine ant Linepithema humile. Mol Ecol 9:119–126PubMedGoogle Scholar
  100. Kropotkin P (1902) Mutual aid: a factor of evolution. William Heinemann, LondonGoogle Scholar
  101. Lacy RC (1980) The evolution of eusociality in termites: a haplodiploid analogy? Am Nat 116:449–451CrossRefGoogle Scholar
  102. Leigh EG (1983) When does the good of the group override the advantage of the individual? Proc Natl Acad Sci USA 80:2985–2989Google Scholar
  103. Leigh EG (1991) Genes, bees and ecosystems: the evolution of a common interest among individuals. Trends Ecol Evol 6:257–262CrossRefGoogle Scholar
  104. Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 14:131–159CrossRefGoogle Scholar
  105. Lindauer M (1954) Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z Vergl Physiol 36:391–432Google Scholar
  106. Lüscher M (1956) Die Entstehung von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis (Frabr.). Insectes Soc 3:119–128Google Scholar
  107. Lüscher M (1961) Air-conditioned termite nests. Sci Am 204(1):138–145Google Scholar
  108. Majerus M, Amos W, Hurst G (1996) Evolution: the four billion year war. Longman, Harlow, UKGoogle Scholar
  109. Martin SJ, Beekman M, Wossler TC, Ratnieks FLW (2002) Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature 415:163–165CrossRefPubMedGoogle Scholar
  110. Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1146Google Scholar
  111. Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. WH Freeman, OxfordGoogle Scholar
  112. Mayr E (1997a) The objects of selection. Proc Natl Acad Sci USA 94:2091–2094CrossRefPubMedGoogle Scholar
  113. Mayr E (1997b) This is biology. Belknap, Harvard University Press, Cambridge, Mass.Google Scholar
  114. Mehdiabadi N, Reeve HK, Mueller UG (2003) Queens versus workers: sex-ratio conflict in eusocial Hymenoptera. Trends Ecol Evol 18:88–93CrossRefGoogle Scholar
  115. Mercot H, Atlan A, Jacques M, Montchamp-Moreau C (1995) Sex-ratio distortion in Drosophila simulans: co-occurrence of a meiotic drive and a suppressor of drive. J Evol Biol 8:283–300Google Scholar
  116. Michod RE (1999) Individuality, immortality, and sex. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 53–74Google Scholar
  117. Michod RE, Roze D (1997) Transitions in individuality. Proc R Soc Lond B 264:853–857CrossRefPubMedGoogle Scholar
  118. Mirenda JT, Vinson SB (1981) Division of labor and specification of castes in the red imported fire ant Solenopsis invicta. Anim Behav 29:410–420Google Scholar
  119. Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108CrossRefGoogle Scholar
  120. Moritz RFA, Southwick EE (1992) Bees as superorganisms: an evolutionary reality. Springer, Berlin Heidelberg New YorkGoogle Scholar
  121. Mueller UG (1991) Haplodiploidy and the evolution of facultative sex ratios in a primitively eusocial bee. Science 254:442–444Google Scholar
  122. Murakami T, Higashi S, Windsor D (2000) Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini). Behav Ecol Sociobiol 48:276–284CrossRefGoogle Scholar
  123. Neumann P, Moritz RFA (2000) Testing genetic variance hypotheses for the evolution of polyandry in the honeybee (Apis mellifera L.). Insectes Soc 41:271–279Google Scholar
  124. Neumann P, Radloff SE, Moritz RFA, Hepburn HR, Reece SL (2001) Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies. Behav Ecol 12:419–428CrossRefGoogle Scholar
  125. Noirot C, Darlington JPEC (2000) Termite nests: architecture, regulation and defence. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, The Netherlands, pp 121–140Google Scholar
  126. Nonacs P (1986) Sex-ratio determination within colonies of ants. Evolution 40:199–204Google Scholar
  127. Nunney L (1999) Lineage selection: natural selection for long-term benefit. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 238–252Google Scholar
  128. Oldroyd BP (2002) The Cape honeybee: an example of a social cancer. Trends Ecol Evol 17:249–251CrossRefGoogle Scholar
  129. Oster GF, Wilson EO (1978) Caste and ecology of social insects. Princeton University Press, Princeton, N.J.Google Scholar
  130. Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honey-bee colonies. Nature 338:576–579CrossRefGoogle Scholar
  131. Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396CrossRefGoogle Scholar
  132. Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 31:235–248CrossRefGoogle Scholar
  133. Peeters C (1991) The occurrence of sexual production among ant workers. Biol J Linn Soc 44:141–152Google Scholar
  134. Peeters C, Higashi S (1989) Reproductive dominance controlled by mutilation in the queenless ant Diacamma australe. Naturwissenschaften 76:177–180Google Scholar
  135. Peters JM, Queller DC, Imperatriz-Fonseca VL, Roubik DW, Strassmann JE (1999) Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc R Soc Lond B 266:379–384CrossRefGoogle Scholar
  136. Pirk CWW, Neumann P, Ratnieks FLW (2003) Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav Ecol 14:347–352CrossRefGoogle Scholar
  137. Pomiankowski A (1999) Intragenomic conflict. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 121–152Google Scholar
  138. Price GR (1970) Selection and covariance. Nature 277:520–421Google Scholar
  139. Price GR (1972) Extension of covariance selection mathematics. Ann Hum Genet 35:485–490PubMedGoogle Scholar
  140. Queller DC (1989) The evolution of eusociality: reproductive head starts of workers. Proc Natl Acad Sci USA 86:3224–3226Google Scholar
  141. Queller DC (1992) Quantitative genetics, inclusive fitness, and group selection. Am Nat 139:540–558CrossRefGoogle Scholar
  142. Queller DC (1994) Extended parental care and the origin of eusociality. Proc R Soc London B 256:105–111Google Scholar
  143. Queller DC (2000) Pax Argentinica. Nature 405:519–520CrossRefPubMedGoogle Scholar
  144. Queller DC, Strassmann JE (1998) Kin selection and social insects. BioScience 48:165–178Google Scholar
  145. Queller DC, Strassmann JE, Hughes C (1993) Microsatellites and kinship. Trends Ecol Evol 8:285–288CrossRefGoogle Scholar
  146. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  147. Ratnieks FLW (1993) Egg laying, egg removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198Google Scholar
  148. Ratnieks FLW, Reeve HK (1992) Conflict in single-queen Hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J Theor Biol 158:33–65Google Scholar
  149. Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797CrossRefGoogle Scholar
  150. Reeve HK (1998) Game theory, reproductive skew, and nepotism. In: Dugatkin LA, Reeve HK (eds) Theory and animal behaviour. Oxford University Press, Oxford, pp 118–145Google Scholar
  151. Reeve HK, Keller L (1999) Levels of selection: burying the units-of-selection debate and unearthing the crucial new issues. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 3–14Google Scholar
  152. Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA “fingerprinting” reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Natl Acad Sci USA 87:2496–2500PubMedGoogle Scholar
  153. Reeve HK, Starks PT, Peters JM, Nonacs P (2000) Genetic support for the evolutionary theory of reproductive transactions in social wasps. Proc R Soc Lond B 267:75–79CrossRefPubMedGoogle Scholar
  154. Robinson GE (1992) Regulation of division of labor in insect colonies. Annu Rev Entomol 37:637–655PubMedGoogle Scholar
  155. Robinson GE, Page RE Jr (1989) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting by honey bee colonies. Behav Ecol Sociobiol 24:317–323Google Scholar
  156. Rosenheim JA, Nonacs P, Mangel M (1996) Sex ratios and multifaceted parental investment. Am Nat 148:501–535CrossRefGoogle Scholar
  157. Sanetra M, Crozier RH (2001) Polyandry and colony genetic structure in the primitive ant Nothomyrmecia macrops. J Evol Biol 14:368–378CrossRefGoogle Scholar
  158. Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553Google Scholar
  159. Seeley TD (1995) The wisdom of the hive. Harvard University Press, Cambridge, Mass.Google Scholar
  160. Seeley TD (1997) Honey bee colonies are group-level adaptive units. Am Nat 150: S22–S41CrossRefGoogle Scholar
  161. Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602–610CrossRefGoogle Scholar
  162. Sober E, Wilson DS (2002) Perspectives and parameterizations: Commentary on Benjamin Kerr and Peter Godfrey-Smith’s “Individualist and multi-level perspectives on selection in structured populations”. Biol Philos 17:529–537CrossRefGoogle Scholar
  163. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, CambridgeGoogle Scholar
  164. Sundström L (1994) Sex ratio bias, relatedness asymmetry and queen mating frequency in ants. Nature 367:266–268CrossRefGoogle Scholar
  165. Sundström L, Chapuisat M, Keller L (1996) Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274:993–995PubMedGoogle Scholar
  166. Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B 270:99–103CrossRefPubMedGoogle Scholar
  167. Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92PubMedGoogle Scholar
  168. Tóth E, Queller DC, Imperatriz-Fonseca VL, Strassmann JE (2002a) Genetic and behavioral conflict over male production between workers and queens in the stingless bee Paratrigona subnuda. Behav Ecol Sociobiol 53:1–8CrossRefGoogle Scholar
  169. Tóth E, Strassmann JE, Nogueira-Neto P, Imperatriz-Fonseca VL, Queller DC (2002b) Male production in stingless bees: variable outcomes of queen–worker conflict. Mol Ecol 11:2261–2267Google Scholar
  170. Tóth E, Strassmann JE, Imperatriz-Fonseca VL, Queller DC (2003) Queens, not workers, produce the males in the stingless bee Schwarziana quadripunctata quadripunctata. Anim Behav 66:359–368CrossRefGoogle Scholar
  171. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263PubMedGoogle Scholar
  172. Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083CrossRefPubMedGoogle Scholar
  173. Uetz GW (2001) Understanding the evolution of social behavior in colonial web-building spiders. In: Dugatkin LA (Ed) Model systems in behavioral ecology. Princeton University Press, Princeton, N.J., pp 110–132Google Scholar
  174. Villesen P, Gertsch PJ, Frydenberg J, Mueller UG, Boomsma JJ (1999) Evolutionary transition from single to multiple mating in fungus-growing ants. Mol Ecol 8:1819–1825CrossRefPubMedGoogle Scholar
  175. Villesen P, Murakami T, Schultz TR, Boomsma JJ (2002) Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc R Soc Lond B 269:1541–1548CrossRefPubMedGoogle Scholar
  176. Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–244CrossRefGoogle Scholar
  177. Wade MJ (1978) Kin selection: a classical approach and a general solution. Proc Natl Acad Sci USA 75:6154–6158Google Scholar
  178. Wade MJ (1979) The evolution of social interactions by family selection. Am Nat 113:399–417CrossRefGoogle Scholar
  179. Wade MJ (1980a) Kin selection: its components. Science 210:665–667Google Scholar
  180. Wade MJ (1980b) An experimental study of kin selection. Evolution 34:844–855Google Scholar
  181. Wade MJ (1982) The effect of multiple inseminations on the evolution of social behavior in diploid and haplodiploid organisms. J Theor Biol 95:351–368PubMedGoogle Scholar
  182. Wade MJ (1985) Soft selection, hard selection, kin selection, and group selection. Am Nat 125:61–73CrossRefGoogle Scholar
  183. Wattanachaiyingcharoen W, Oldroyd BP, Wongsiri S, Palmer K, Paar J (2003) A scientific note on the mating frequency of Apis dorsata Fabricius. Apidologie 34:85–86CrossRefGoogle Scholar
  184. Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474Google Scholar
  185. Wenzel JW (1991) Evolution of nest architecture. In: Ross KG (ed) The social biology of wasps. Cornell University Press, Ithaca, N.Y., pp 480–519Google Scholar
  186. West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33CrossRefGoogle Scholar
  187. Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thoughts. Princeton University Press, Princeton, N.J.Google Scholar
  188. Wilson DS (1997a) Introduction: multilevel selection theory comes of age. Am Nat 150:S1–S4CrossRefGoogle Scholar
  189. Wilson DS (1997b) Altruism and organism: disentangling the themes of multilevel selection theory. Am Nat 150:S122–S134CrossRefGoogle Scholar
  190. Wilson EO (1971) The insect societies. Belknap, Harvard University Press, Cambridge, Mass.Google Scholar
  191. Woyciechowski M, Warakomska Z (1994) Workers’ genetic diversity has no relation to pollen diversity in a honey bee colony (Apis mellifera L.). J Ethol 12:163–167Google Scholar
  192. Woyciechowski M, Król R, Figurny E, Stachowicz M, Tracz M (1994) Genetic diversity of workers and infection by the parasite Nosema apis in honey bee colonies (Apis mellifera L). In: Lenoir A, Arnold G, Lepage M (eds) Les insectes sociaux. Université Paris Nord, Paris, p 347Google Scholar
  193. Wynne-Edwards VC (1962) Animal dispersion in relation to social behavior. Oliver and Boyd, EdinburghGoogle Scholar
  194. Yasui Y (1998) The ‘genetic benefits” of female multiple mating revisited. Trends Ecol Evol 13:246–250Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Biologie IUniversität RegensburgRegensburgGermany

Personalised recommendations