Skip to main content
Log in

Multilevel selection and social evolution of insect societies

  • Review
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4a, b
Fig. 5

Similar content being viewed by others

References

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  • Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237

    CAS  Google Scholar 

  • Anderson C, Ratnieks FLW (1999) Task partitioning in insect societies. I. Effect of colony size on queuing delay and colony ergonomic efficiency. Am Nat 154:521–535

    PubMed  Google Scholar 

  • 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 53–65

  • Atlan A, Mercot H, Landre C, Montchamp-Moreau C (1997) The sex-ratio trait in Drosophila simulans: geographical distribution of distortion and resistance. Evolution 51:1886–1895

    Google Scholar 

  • Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite load and fitness in a bumble-bee. Nature 397:151–153

    CAS  Google Scholar 

  • Banschbach VA, Herbers JM (1996) Complex colony structure in social insects. II. Reproduction, queen-worker conflict, and levels of selection. Evolution 50:298–307

    Google Scholar 

  • Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci USA 76:5764–5768

    Google Scholar 

  • Beekman M, Sumpter DJT, Ratnieks FLW (2001) Phase transition between disordered and ordered foraging in Pharaoh’s ants. Proc Natl Acad Sci USA 98:9703–9706

    Article  CAS  PubMed  Google Scholar 

  • Beekman M, Komdeur J, Ratnieks FLW (2003) Reproductive conflicts in social animals: who has power? Trends Ecol Evol 188:277–282

    Article  Google Scholar 

  • Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440

    CAS  PubMed  Google Scholar 

  • Bonabeau E, Theraulaz G, Deneubourg JL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 12:188–193

    Article  Google Scholar 

  • Boomsma JJ, Grafen A (1990) Intraspecific variation in ant sex ratios and the Trivers–Hare hypothesis. Evolution 44:1026–1034

    Google Scholar 

  • Boomsma JJ, Grafen A (1991) Colony-level sex ratio selection in the eusocial Hymenoptera. J Evol Biol 3:383–407

    Google Scholar 

  • Boomsma JJ, Ratnieks FLW (1996) Paternity in social Hymenoptera. Philos Trans R Soc Lond B 351:947–975

    Google Scholar 

  • Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311

    Article  Google Scholar 

  • Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257

    Article  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.

  • Braude S (2000) Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating. Behav Ecol 11:7–12

    Article  Google Scholar 

  • 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 267:1751–1757

    CAS  PubMed  Google Scholar 

  • Brown WD, Keller L, Sundström L (2002) Sex allocation in mound-building ants: the roles of resources and queen replenishment. Ecology 83:1945–1952

    Google Scholar 

  • Buss L (1987) The evolution of individuality. Princeton University Press, Princeton, N.J.

  • Camazine S, Deneubourg JL, Franks N, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton, N.J.

  • Chan GL, Hingle A, Bourke AFG (1999) Sex allocation in a facultatively polygynous ant: between-population and between-colony variation. Behav Ecol 10:409–421

    Article  Google Scholar 

  • 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 97:1648–1650

    Article  CAS  PubMed  Google Scholar 

  • Choe JC (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. Brill, Leiden, pp 163–187

  • Cockburn A (1998) Evolution of helping behaviour in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177

    Google Scholar 

  • 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 61:238–244

    Google Scholar 

  • Crozier RH, Fjerdingstad EJ (2001) Polyandry in social Hymenoptera: disunity in diversity? Ann Zool Fenn 38:267–285

    Google Scholar 

  • Crozier RH, Luykx P (1985) The evolution of termite eusociality is unlikely to have been based on a male-haploid analogy. Am Nat 126:867–869

    Article  Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford

    Google Scholar 

  • 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 269:1295–1300

    Article  PubMed  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. John Murray, London

  • Darwin C (1871) The descent of man and selection in relation to sex. Appleton, New York

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

  • 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 1–76

  • Dugatkin LA, Reeve HK (1994) Behavioral ecology and levels of selection: dissolving the group selection controversy. Adv Stud Behav 23:101–133

    Google Scholar 

  • Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology, 4th edn. Blackwell Science, Oxford, pp 228–253

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford

  • Fjerdingstad EJ (2004) Multiple paternity and colony homeostasis in Lasius niger ants. Behav Ecol Sociobiol 55: 10.1007/s00265-004-0759-8

    Google Scholar 

  • 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 56:553–562

    PubMed  Google Scholar 

  • Foitzik S, Heinze J (2000) Intraspecific parasitism and split sex ratios in a monogynous, monandrous ant (Leptothorax nylanderi). Behav Ecol Sociobiol 47:424–431

    Article  Google Scholar 

  • Foitzik S, Herbers JM (2001) Colony structure of a slavemaking ant. I. Intracolony relatedness, worker reproduction, and polydomy. Evolution 55:307–315

    CAS  PubMed  Google Scholar 

  • Foitzik S, Strätz M, Heinze J (2003) Ecology, life history, and resource allocation in the ant, Leptothorax nylanderi. J Evol Biol 16:670–680

    Article  Google Scholar 

  • Foster KR, Gulliver J, Ratnieks FLW (2002) Why workers do not reproduce: worker policing in the European hornet Vespa crabro. Insectes Soc 49:41–44

    Article  Google Scholar 

  • 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 57:1336–1342

    PubMed  Google Scholar 

  • Frank SA (1985) Hierarchical selection theory and sex ratio. II. On applying the theory, and a test with fig wasps. Evolution 39:949–964

    Google Scholar 

  • Frank SA (1990) Sex allocation theory for birds and mammals. Annu Rev Ecol Syst 21:13–55

    Article  Google Scholar 

  • Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78

    CAS  PubMed  Google Scholar 

  • Frank SA (1997) Foundations of social evolution. Princeton University Press, Princeton, N.J.

  • 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 357:1567–1583

    Article  Google Scholar 

  • Frumhoff PC, Baker J (1988) A genetic component to the division of labour within honey bee colonies. Nature 333:358–361

    Article  Google Scholar 

  • Fuchs S, Schade V (1994) Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155–168

    Google Scholar 

  • Gadagkar R (1985) Evolution of insect sociality: a review of some attempts to test modern theories. Proc Indian Acad Sci (Anim Sci) 94:309–324

    Google Scholar 

  • Gadagkar R (1990) Evolution of eusociality: the advantage of assured fitness returns. Philos Trans R Soc Lond B 329:17–25

    Google Scholar 

  • 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 12:1931–1938

    Article  CAS  PubMed  Google Scholar 

  • Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079

    CAS  PubMed  Google Scholar 

  • Goodnight CJ, Stevens L (1997) Experimental studies of group selection: what do they tell us about group selection in nature? Am Nat 150:S59–S79

    Article  Google Scholar 

  • Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124

    CAS  Google Scholar 

  • Grafen A (1984) Natural selection, kin selection and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology, 2nd edn. Blackwell Science, Oxford, pp 62–84

  • 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 351:617–625

    Google Scholar 

  • Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636

    Article  CAS  PubMed  Google Scholar 

  • Haldane JBS (1932) The causes of evolution. Longmans Green, London

  • Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 97:354–356

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. I, II. J Theor Biol 7:1–52

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1970) Selfish and spiteful behaviour in an evolutionary model. Nature 228:1218–1220

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232

    Article  Google Scholar 

  • Hamilton WD (1975) Innate social aptitudes in man: an approach from evolutionary genetics. In: Fox R (ed) Biosocial anthropology. Malaby, London, pp 133–155

  • Hammond RL, Bruford MW, Bourke AFG (2002) Ant workers selfishly bias sex ratios by manipulating female development. Proc R Soc Lond B 269:173–178

    Article  CAS  Google Scholar 

  • Hammond RL, Bruford MW, Bourke AFG (2003) Male parentage does not vary with colony kin structure in a multiple-queen ant. J Evol Biol 16:446–455

    CAS  PubMed  Google Scholar 

  • Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–2429

    PubMed  Google Scholar 

  • Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci USA 100:12836–12840

    Article  CAS  PubMed  Google Scholar 

  • Heinrich B (1993) The hot-blooded insect. Harvard University Press, Cambridge, Mass.

  • Heinze J (1995) Reproductive skew and relatedness in Leptothorax ants. Proc R Soc Lond B 261:375–379

    Google Scholar 

  • Heinze J (1996) The reproductive potential of workers in slave-making ants. Insectes Soc 43:319–328

    Google Scholar 

  • Heinze J, Hölldobler B (1995) Thelytokous parthenogenesis and dominance hierarchies in the ponerine ant, Platythyrea punctata (F. Smith). Naturwissenschaften 82:40–41

    Article  CAS  Google Scholar 

  • Heinze J, Cover SP, Hölldobler B (1995) Neither worker nor queen: an ant caste specialized on the production of male eggs. Psyche 102:173–185

    Google Scholar 

  • Heinze J, Strätz M, Pedersen JS, Haberl M (2000) Microsatellite analysis suggests occasional worker reproduction in the monogynous ant Crematogaster smithi. Insectes Soc 47:299–301

    Google Scholar 

  • Helms KR (1999) Colony sex ratios, conflict between queens and workers, and apparent queen control in the ant Pheidole desertorum. Evolution 53:1470–1478

    Google Scholar 

  • 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 314–330

  • 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 238–242

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, Mass.

  • Horstmann K (1983) Regulation der Temperatur in Waldameisennestern (Formica polyctena Förster). Z Naturforsch 38:508–510

    Google Scholar 

  • Horstmann K (1990) Zur Entstehung des Wärmezentrums in Waldameisennestern (Formica polyctena Förster; Hymenoptera, Formicidae). Zool Beitr NF 33:105–124

    Google Scholar 

  • Iwanishi S, Hasegawa E, Ohkawara K (2003) Worker oviposition and policing behaviour in the myrmicine ant Aphaenogaster smythiesi japonica Forel. Anim Behav 66:513–519

    Article  Google Scholar 

  • Jeanne R (1975) The adaptiveness of social wasp nest architecture. Q Rev Biol 50:267–287

    Article  Google Scholar 

  • Jeon J, Choe JC (2003) Reproductive skew and the origin of sterile castes. Am Nat 161:206–224

    Article  PubMed  Google Scholar 

  • 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 96:8665–8669

    Article  Google Scholar 

  • Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 146:610–632

    Article  Google Scholar 

  • Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Evol Ecol 10:355–360

    Article  Google Scholar 

  • Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. Trend Ecol Evol 12:99–103

    Article  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects; queen control or queen signal? Anim Behav 45:787–794

    Google Scholar 

  • Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704

    Google Scholar 

  • Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291–315

    Google Scholar 

  • 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 153–175

  • Korb J (2003) Thermoregulation and ventilation of termite mounds. Naturwissenschaften 90:212–219

    CAS  PubMed  Google Scholar 

  • Korb J, Linsenmair KE (2000) Ventilation of termite mounds: new results require a new model. Behav Ecol 11:486–494

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

  • Krieger MJB, Keller L (2000) Mating frequency and genetic structure of the Argentine ant Linepithema humile. Mol Ecol 9:119–126

    CAS  PubMed  Google Scholar 

  • Kropotkin P (1902) Mutual aid: a factor of evolution. William Heinemann, London

    Google Scholar 

  • Lacy RC (1980) The evolution of eusociality in termites: a haplodiploid analogy? Am Nat 116:449–451

    Article  Google Scholar 

  • Leigh EG (1983) When does the good of the group override the advantage of the individual? Proc Natl Acad Sci USA 80:2985–2989

    Google Scholar 

  • Leigh EG (1991) Genes, bees and ecosystems: the evolution of a common interest among individuals. Trends Ecol Evol 6:257–262

    Article  Google Scholar 

  • Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 14:131–159

    Article  Google Scholar 

  • Lindauer M (1954) Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z Vergl Physiol 36:391–432

    Google Scholar 

  • Lüscher M (1956) Die Entstehung von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis (Frabr.). Insectes Soc 3:119–128

    Google Scholar 

  • Lüscher M (1961) Air-conditioned termite nests. Sci Am 204(1):138–145

    CAS  Google Scholar 

  • Majerus M, Amos W, Hurst G (1996) Evolution: the four billion year war. Longman, Harlow, UK

  • Martin SJ, Beekman M, Wossler TC, Ratnieks FLW (2002) Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature 415:163–165

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1146

    Google Scholar 

  • Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. WH Freeman, Oxford

  • Mayr E (1997a) The objects of selection. Proc Natl Acad Sci USA 94:2091–2094

    Article  CAS  PubMed  Google Scholar 

  • Mayr E (1997b) This is biology. Belknap, Harvard University Press, Cambridge, Mass.

  • Mehdiabadi N, Reeve HK, Mueller UG (2003) Queens versus workers: sex-ratio conflict in eusocial Hymenoptera. Trends Ecol Evol 18:88–93

    Article  Google Scholar 

  • 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 8:283–300

    Google Scholar 

  • Michod RE (1999) Individuality, immortality, and sex. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 53–74

  • Michod RE, Roze D (1997) Transitions in individuality. Proc R Soc Lond B 264:853–857

    Article  CAS  PubMed  Google Scholar 

  • Mirenda JT, Vinson SB (1981) Division of labor and specification of castes in the red imported fire ant Solenopsis invicta. Anim Behav 29:410–420

    Google Scholar 

  • Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108

    Article  Google Scholar 

  • Moritz RFA, Southwick EE (1992) Bees as superorganisms: an evolutionary reality. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Mueller UG (1991) Haplodiploidy and the evolution of facultative sex ratios in a primitively eusocial bee. Science 254:442–444

    Google Scholar 

  • Murakami T, Higashi S, Windsor D (2000) Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini). Behav Ecol Sociobiol 48:276–284

    Article  Google Scholar 

  • Neumann P, Moritz RFA (2000) Testing genetic variance hypotheses for the evolution of polyandry in the honeybee (Apis mellifera L.). Insectes Soc 41:271–279

    Google Scholar 

  • 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 12:419–428

    Article  Google Scholar 

  • 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 121–140

  • Nonacs P (1986) Sex-ratio determination within colonies of ants. Evolution 40:199–204

    Google Scholar 

  • 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 238–252

  • Oldroyd BP (2002) The Cape honeybee: an example of a social cancer. Trends Ecol Evol 17:249–251

    Article  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology of social insects. Princeton University Press, Princeton, N.J.

  • Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honey-bee colonies. Nature 338:576–579

    Article  Google Scholar 

  • 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 36:387–396

    Article  Google Scholar 

  • Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 31:235–248

    Article  Google Scholar 

  • Peeters C (1991) The occurrence of sexual production among ant workers. Biol J Linn Soc 44:141–152

    Google Scholar 

  • Peeters C, Higashi S (1989) Reproductive dominance controlled by mutilation in the queenless ant Diacamma australe. Naturwissenschaften 76:177–180

    Google Scholar 

  • 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 266:379–384

    Article  Google Scholar 

  • Pirk CWW, Neumann P, Ratnieks FLW (2003) Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav Ecol 14:347–352

    Article  Google Scholar 

  • Pomiankowski A (1999) Intragenomic conflict. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 121–152

  • Price GR (1970) Selection and covariance. Nature 277:520–421

    Google Scholar 

  • Price GR (1972) Extension of covariance selection mathematics. Ann Hum Genet 35:485–490

    CAS  PubMed  Google Scholar 

  • Queller DC (1989) The evolution of eusociality: reproductive head starts of workers. Proc Natl Acad Sci USA 86:3224–3226

    Google Scholar 

  • Queller DC (1992) Quantitative genetics, inclusive fitness, and group selection. Am Nat 139:540–558

    Article  Google Scholar 

  • Queller DC (1994) Extended parental care and the origin of eusociality. Proc R Soc London B 256:105–111

    Google Scholar 

  • Queller DC (2000) Pax Argentinica. Nature 405:519–520

    Article  CAS  PubMed  Google Scholar 

  • Queller DC, Strassmann JE (1998) Kin selection and social insects. BioScience 48:165–178

    Google Scholar 

  • Queller DC, Strassmann JE, Hughes C (1993) Microsatellites and kinship. Trends Ecol Evol 8:285–288

    Article  Google Scholar 

  • Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236

    Article  Google Scholar 

  • Ratnieks FLW (1993) Egg laying, egg removal, and ovary development by workers in queenright honey bee colonies. Behav Ecol Sociobiol 32:191–198

    Google Scholar 

  • 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 158:33–65

    Google Scholar 

  • Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797

    Article  Google Scholar 

  • Reeve HK (1998) Game theory, reproductive skew, and nepotism. In: Dugatkin LA, Reeve HK (eds) Theory and animal behaviour. Oxford University Press, Oxford, pp 118–145

  • 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 3–14

  • 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 87:2496–2500

    CAS  PubMed  Google Scholar 

  • 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 267:75–79

    Article  CAS  PubMed  Google Scholar 

  • Robinson GE (1992) Regulation of division of labor in insect colonies. Annu Rev Entomol 37:637–655

    CAS  PubMed  Google Scholar 

  • Robinson GE, Page RE Jr (1989) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting by honey bee colonies. Behav Ecol Sociobiol 24:317–323

    Google Scholar 

  • Rosenheim JA, Nonacs P, Mangel M (1996) Sex ratios and multifaceted parental investment. Am Nat 148:501–535

    Article  Google Scholar 

  • Sanetra M, Crozier RH (2001) Polyandry and colony genetic structure in the primitive ant Nothomyrmecia macrops. J Evol Biol 14:368–378

    Article  Google Scholar 

  • Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553

    Google Scholar 

  • Seeley TD (1995) The wisdom of the hive. Harvard University Press, Cambridge, Mass.

  • Seeley TD (1997) Honey bee colonies are group-level adaptive units. Am Nat 150: S22–S41

    Article  Google Scholar 

  • Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602–610

    Article  Google Scholar 

  • 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 17:529–537

    Article  Google Scholar 

  • Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, Cambridge

  • Sundström L (1994) Sex ratio bias, relatedness asymmetry and queen mating frequency in ants. Nature 367:266–268

    Article  Google Scholar 

  • Sundström L, Chapuisat M, Keller L (1996) Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274:993–995

    PubMed  Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B 270:99–103

    Article  PubMed  Google Scholar 

  • Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92

    CAS  PubMed  Google Scholar 

  • 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 53:1–8

    Article  Google Scholar 

  • 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 11:2261–2267

    Google Scholar 

  • 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 66:359–368

    Article  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263

    CAS  PubMed  Google Scholar 

  • Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083

    Article  CAS  PubMed  Google Scholar 

  • 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 110–132

  • Villesen P, Gertsch PJ, Frydenberg J, Mueller UG, Boomsma JJ (1999) Evolutionary transition from single to multiple mating in fungus-growing ants. Mol Ecol 8:1819–1825

    Article  CAS  PubMed  Google Scholar 

  • 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 269:1541–1548

    Article  PubMed  Google Scholar 

  • Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–244

    Article  Google Scholar 

  • Wade MJ (1978) Kin selection: a classical approach and a general solution. Proc Natl Acad Sci USA 75:6154–6158

    Google Scholar 

  • Wade MJ (1979) The evolution of social interactions by family selection. Am Nat 113:399–417

    Article  Google Scholar 

  • Wade MJ (1980a) Kin selection: its components. Science 210:665–667

    Google Scholar 

  • Wade MJ (1980b) An experimental study of kin selection. Evolution 34:844–855

    Google Scholar 

  • Wade MJ (1982) The effect of multiple inseminations on the evolution of social behavior in diploid and haplodiploid organisms. J Theor Biol 95:351–368

    CAS  PubMed  Google Scholar 

  • Wade MJ (1985) Soft selection, hard selection, kin selection, and group selection. Am Nat 125:61–73

    Article  Google Scholar 

  • Wattanachaiyingcharoen W, Oldroyd BP, Wongsiri S, Palmer K, Paar J (2003) A scientific note on the mating frequency of Apis dorsata Fabricius. Apidologie 34:85–86

    Article  Google Scholar 

  • Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474

    Google Scholar 

  • Wenzel JW (1991) Evolution of nest architecture. In: Ross KG (ed) The social biology of wasps. Cornell University Press, Ithaca, N.Y., pp 480–519

  • West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thoughts. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Wilson DS (1997a) Introduction: multilevel selection theory comes of age. Am Nat 150:S1–S4

    Article  Google Scholar 

  • Wilson DS (1997b) Altruism and organism: disentangling the themes of multilevel selection theory. Am Nat 150:S122–S134

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap, Harvard University Press, Cambridge, Mass.

  • Woyciechowski M, Warakomska Z (1994) Workers’ genetic diversity has no relation to pollen diversity in a honey bee colony (Apis mellifera L.). J Ethol 12:163–167

    Google Scholar 

  • 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 347

  • Wynne-Edwards VC (1962) Animal dispersion in relation to social behavior. Oliver and Boyd, Edinburgh

  • Yasui Y (1998) The ‘genetic benefits” of female multiple mating revisited. Trends Ecol Evol 13:246–250

    Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Judith Korb.

Additional information

Dedicated to Prof. Ernst Mayr

Rights and permissions

Reprints and permissions

About this article

Cite this article

Korb, J., Heinze, J. Multilevel selection and social evolution of insect societies. Naturwissenschaften 91, 291–304 (2004). https://doi.org/10.1007/s00114-004-0529-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-004-0529-5

Keywords

Navigation