Skip to main content

Eusocial Evolution in Termites and Hymenoptera

  • Chapter
  • First Online:
Biology of Termites: a Modern Synthesis

Abstract

The evolution of eusociality remains an intriguing mystery. Why do individuals forego their own reproduction to help others produce offspring? Complex colonies have evolved in ants, bees, and wasps (Hymenoptera) and in termites (Isoptera). We discuss theories applied to explain eusocial traits in the Isoptera and the Hymenoptera in order to learn more about how and why eusociality evolved from subsocial ancestors. Striking overlap occurs in the genes controlling caste and the shift of parental care to offspring via heterochrony, suggesting ecological pressures lead to co-option of similar developmental mechanisms. There is also overlap in factors that predispose groups to eusociality, including extended parental care, defense of and the inheritance of a valuable nest, and enhanced direct and indirect benefits from cooperative behavior. However, differences in developmental paths and ecological traits are also informative, such as the evolution of the soldier form and adult workers. Multiple selective processes may favor eusociality over alternatives, but the degree to which each process was involved in eusocial evolution may have varied in each taxon. Reduced emphasis on haplodiploidy to explain eusocial evolution in the Hymenoptera and the similarities in developmental control allow for greater overlap of theories explaining eusocial evolution in the Hymenoptera and Isoptera.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 125–148

    Google Scholar 

  • Abe T (1991) Ecological factors associated with the evolution of worker and soldier castes in termites. Ann Entomol 9:101–107

    Google Scholar 

  • Alcock J, Sherman P (1994) The utility of the proximate-ultimate dichotomy in ethology. Ethology 96:58–62

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Alexander RD, Noonan KM, Crespi BJ (1991) The evolution of eusociality. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the Naked Mole-rat. Princeton University Press, Princeton, NJ, pp 3–44

    Google Scholar 

  • Alonso WJ, Schuck-Paim C (2002) Sex-ratio conflicts, kin selection, and the evolution of altruism. Proc Natl Acad Sci U S A 99:6843–6847

    Article  PubMed  CAS  Google Scholar 

  • Amdam GV, Csondes A, Fondrk MK, Page RE (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439:76–78

    Article  PubMed  CAS  Google Scholar 

  • Andersson M (1984) The evolution of eusociality. Annu Rev Ecol Syst 15:165–189

    Google Scholar 

  • Atkinson L, Adams ES (1997) The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proc R Soc Lond B 264:1131–1136

    Article  Google Scholar 

  • Atkinson L, Teschendorf G, Adams ES (2008) Lack of evidence for nepotism by workers tending queens of the polygynous termite Nasutitermes corniger. Behav Ecol Sociobiol 62:805–812

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Basalingappa S (1970) Environmental hazards to reproductives of Odontotermes assmuthi Holmgren. Indian Zool 1:45–50

    Google Scholar 

  • Bloch G, Hefetz A (1999) Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies. Behav Ecol Sociobiol 45:125–135

    Article  Google Scholar 

  • Boomsma JJ (2007) Kin selection versus sexual selection: why the ends do not meet. Curr Biol 17:673–683

    Article  CAS  Google Scholar 

  • Boomsma JJ (2009) Lifetime monogamy and the evolution of eusociality. Phil Trans R Soc Lond B 364:1–17

    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 (2005) Genetics, relatedness and social behaviour in insect societies. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. Proceedings of the Royal Entomological Society, 22nd Symposium. CABI Publishing, Cambridge, Massachusetts, pp 1–30

    Chapter  Google Scholar 

  • Bourke AFG (2007) Social evolution: community policing in insects. Curr Biol 17:519–520

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci U S A 103:18172–18177

    Article  PubMed  CAS  Google Scholar 

  • Breed MD, Guzm´an-Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other social insects. Annu Rev Entomol 49:271–298

    Article  PubMed  CAS  Google Scholar 

  • Brian MV (1973) Caste control through worker attack in the ant Myrmica. Insectes Soc 20:87–102

    Article  Google Scholar 

  • Broughton RE (1995) Mitochondrial DNA variation within and among species of termites in the genus Zootermopsis (Isoptera: Termopsidae). Ann Entomol Soc Am 88:120–128

    Google Scholar 

  • Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243

    Article  Google Scholar 

  • Buston PM, Zink AG (2009) Reproductive skew and the evolution of conflict resolution: a synthesis of transactional and tug-of-war models. Behav Ecol 20:672–684

    Article  Google Scholar 

  • Charnov EL (1978) Evolution of eusocial behavior: offspring choice or parental parasitism? J Theor Biol 75:451

    Article  PubMed  CAS  Google Scholar 

  • Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, MA

    Book  Google Scholar 

  • Clément JL (1986) Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae): geographic and seasonal variations. Sociobiology 11:311–323

    Google Scholar 

  • Cleveland LR, Hall SR, Sanders EP, Collier J (1934) The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem Am Acad Arts Sci 17:185–342

    Google Scholar 

  • Collins NM (1983) The utilization of nitrogen resources by termites (Isoptera). In: Lee JA, McNeill S, Rorison IH (eds) Nitrogen as an ecological factor. Blackwell Scientific Publications, Oxford, pp 381–412

    Google Scholar 

  • Craig R (1979) Parental manipulation, kin selection, and the evolution of altruism. Evolution 33:319–334

    Article  Google Scholar 

  • Craig R (1982) Evolution of male workers in the Hymenoptera. J Theor Biol 94:95–105

    Article  Google Scholar 

  • Craig R (1983) Subfertility and the evolution of eusociality by kin selection. J Theor Biol 100:379–397

    Article  Google Scholar 

  • Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insectes Soc 41:395–400

    Article  Google Scholar 

  • Crespi BJ (1996) Comparative analysis of the origins and losses of eusociality: causal mosaics and historical uniqueness. In: Martins E (ed) Phylogenies and the comparative method in animal behavior. Oxford University Press, New York, pp 253–287

    Google Scholar 

  • Crespi BJ, Ragsdale JE (2000) A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved. Proc Biol Sci 267:821–828

    Article  PubMed  CAS  Google Scholar 

  • Crosland MWJ, Crozier RH (1986) Myrmecia pilosula, an ant with only one pair of chromosomes. Science 231:1278

    Article  PubMed  CAS  Google Scholar 

  • Crozier RH (2008) Advanced eusociality, kin selection and male haploidy. Aust J Entomol 47:2–8

    Article  Google Scholar 

  • Crozier RH, Jermiin LS, Chiotis M (1997) Molecular evidence for a Jurassic origin of ants. Naturwissenschaften 84:22–23

    Article  CAS  Google Scholar 

  • DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441

    Article  PubMed  Google Scholar 

  • Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381:512–514

    Article  CAS  Google Scholar 

  • Field J, Foster W (1999) Helping behaviour in facultatively eusocial hover wasps: an experimental test of the subfertility hypothesis. Anim Behav 57:633–636

    Article  PubMed  Google Scholar 

  • Field J, Shreeves G, Sumner S, Casiraghi M (2000) Insurance-based advantage to helpers in a tropical hover wasp. Nature 404:869–871

    Article  PubMed  CAS  Google Scholar 

  • Fjerdingstad EJ, Crozier RH (2006) The evolution of worker caste diversity in social insects. Am Nat 167:390–400

    Article  PubMed  Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343

    Article  Google Scholar 

  • Foster KR, Wenseleers T, Ratnieks FLW (2006) Kin selection is the key to altruism. Trends Ecol Evol 21:57–60

    Article  PubMed  Google Scholar 

  • Fraser VS, Kaufmann B, Oldroyd BP, Crozier RH (2000) Genetic influence on caste in the ant Camponotus consobrinus. Behav Ecol Sociobiol 47:188–194

    Article  Google Scholar 

  • Gadagkar R (1991a) On testing the role of genetic asymmetries created by haplodiploidy in the evolution of eusociality in the Hymenoptera. J Genet 70:1–31

    Article  Google Scholar 

  • Gadagkar R (1991b) Demographic predisposition to the evolution of eusociality: a hierarchy of models. Proc Natl Acad Sci U S A 88:10993–10997

    Article  PubMed  CAS  Google Scholar 

  • Gadagkar R (2001) The social biology of Ropalidia marginata: toward understanding the evolution of eusociality. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Gadagkar R, Vinutha C, Shanubhogue A, Gore AP (1988) Pre-imaginal biasing of caste in a primitively eusocial insect. Proc R Soc Lond B 233:175–189

    Article  Google Scholar 

  • Gardner A, Foster KR (2008) The evolution and ecology of cooperation – history and concepts. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 1–36

    Chapter  Google Scholar 

  • Gay FJ, Calaby JH (1970) Termites of the Australian region. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, New York, pp 393–448

    Google Scholar 

  • Goodisman MAD, Crozier RH (2002) Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56:70–83

    PubMed  Google Scholar 

  • Grassé PP (1986) Termitologia, vol 3. Masson, Paris

    Google Scholar 

  • Grimaldi DA, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  PubMed  CAS  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 (1978) Evolution and diversity under bark. In: Mound LA, Waloff N (eds) Diversity of insect faunas. Symposium of the Royal Entomological Society of London, vol 9. Halsted, New York, NY, pp 154–175

    Google Scholar 

  • Hansell MH (1987) Nest building as a facilitating and limiting factor in the evolution of eusociality in the Hymenoptera. In: Harvey PH, Partridge L (eds) Oxford surveys in evolutionary biology, vol 4. Oxford University Press, Oxford, pp 155–181

    Google Scholar 

  • Hansell MH (1996) Wasps make nests: nests make conditions. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, Oxford, pp 272–289

    Google Scholar 

  • Hare L (1937) Termite phylogeny as evidenced by soldier mandible development. Ann Entomol Soc Am 30:459–486

    Google Scholar 

  • Hartfelder K, Emlen DJ (2005) Endocrine control of insect polyphenism. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol 3. Elsevier, Oxford, pp 651–703

    Chapter  Google Scholar 

  • Haverty MI (1977) The proportion of soldiers in termite colonies: a list and a bibliography (Isoptera). Sociobiology 2:199–216

    Google Scholar 

  • Hayashi Y, Lo N, Miyata H et al (2007) Sex-linked genetic influence on caste determination in a termite. Science 318:985–987

    Article  PubMed  CAS  Google Scholar 

  • Heath H (1928) Fertile termite soldiers. Biol Bull 54:324–326

    Article  Google Scholar 

  • Heinze J (2008a) Social plasticity: ecology, genetics, and the structure of ant societies. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 129–150

    Chapter  Google Scholar 

  • Heinze J (2008b) The demise of the standard ant. Myrmecol News 11:9–20

    Google Scholar 

  • Helanterä H, Bargum K (2007) Pedigree relatedness, not greenbeard genes, explains eusociality. Oikos 116:217

    Article  Google Scholar 

  • Higashi M, Yamamura N, Abe T, Burns TP (1991) Why don’t all termite species have a sterile worker caste? Proc R Soc Lond B 246:25–29

    Article  CAS  Google Scholar 

  • Higashi M, Yamamura N, Abe T (2000) Theories on the sociality of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 169–188

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The Ants. Belknap Press, Cambridge, MA

    Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216

    Article  PubMed  CAS  Google Scholar 

  • Hunt JH (1991) Nourishment and the evolution of the social Vespidae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 426–450

    Google Scholar 

  • Hunt JH (1994) Nourishment and social evolution in wasps sensu lato. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, CO, pp 211–244

    Google Scholar 

  • Hunt JH (1999) Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution 53:225–237

    Article  Google Scholar 

  • Hunt JH (2007) The evolution of social wasps. Oxford University Press, Oxford

    Book  Google Scholar 

  • Hunt JH, Amdam GV (2005) Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308:264–267

    Article  PubMed  CAS  Google Scholar 

  • Husseneder C, Brandl R, Epplen C et al (1999) Within-colony relatedness in a termite species: genetic roads to eusociality? Behaviour 136:1045–1063

    Article  Google Scholar 

  • Imms AD (1919) On the structure and biology of Archotermopsis, together with descriptions of new species of intestinal protozoa, and general observations on the Isoptera. Phil Trans R Soc Lond 209:75–180

    Google Scholar 

  • Inward DJG, Beccaloni G, Eggleton P (2007a) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331

    Article  PubMed  CAS  Google Scholar 

  • Inward DJG, Vogler AP, Eggleton P (2007b) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44:953–967

    Article  PubMed  CAS  Google Scholar 

  • Jeanne RL (2009) Vibrational signals in social wasps: a role in caste determination? In: Gadau J, Fewell JH (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, MA, 243–265

    Google Scholar 

  • Johns PM, Howard KJ, Breisch NL et al (2009) Nonrelatives inherit colony resources in a primitive termite. Proc Natl Acad Sci U S A 106:17452–17456

    Article  PubMed  CAS  Google Scholar 

  • Julian GE, Fewell JH, Gadau J et al (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci U S A 99:8157–8160

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Kennedy JS (1947) Child labor of the termite society versus adult labor of the ant society. Sci Mon 65:309–324

    Google Scholar 

  • Kerr WE (1950) Evolution of the mechanism of caste determination in the genus Melipona. Evolution 4:7–13

    Article  Google Scholar 

  • Kokko H, Johnstone RA (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B 266:571–578

    Article  Google Scholar 

  • Korb J (2007) Workers of a drywood termite do not work. Front Zool 4:7

    Article  PubMed  Google Scholar 

  • Korb J (2008) The ecology of social evolution in termites. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 151–174

    Chapter  Google Scholar 

  • Korb J, Heinze J (2008) The ecology of social life: a synthesis. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 245–260

    Chapter  Google Scholar 

  • Korb J, Schmidinger S (2004) Help or disperse? Cooperation in termites influenced by food conditions. Behav Ecol Sociobiol 56:89–95

    Article  Google Scholar 

  • Korb J, Schneider K (2007) Does kin structure explain the occurrence of workers in a lower termite? Evol Ecol 21:817–828

    Article  Google Scholar 

  • Kukuk PF, Eickwort GC, Raveret-Richter M et al (1989) Importance of the sting in the evolution of sociality in the Hymenoptera. Ann Entomol Soc Am 82:1–5

    Google Scholar 

  • Kumano N, Kasuya E (2001) Why do workers of the primitively eusocial wasp Polistes chinensis antennalis remain at their natal nest? Anim Behav 61:655–660

    Article  Google Scholar 

  • LaFage JP, Nutting WL (1978) Nutrient dynamics of termites. In: Brian MV (ed) Production ecology of ants and termites. Cambridge University Press, Cambridge, pp 165–244

    Google Scholar 

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

    Article  Google Scholar 

  • Lacy RC (1984) The evolution of termite sociality: reply to Leinaas. Am Nat 123:876–879

    Article  Google Scholar 

  • Legendre F, Whiting MF, Bordereau C et al (2008) The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol Phylogenet Evol 48:615–627

    Article  PubMed  CAS  Google Scholar 

  • Lehmann L, Keller L (2006) The evolution of cooperation and altruism-a general framework and a classification of models. J Evol Biol 19:1365–1376

    Article  PubMed  CAS  Google Scholar 

  • Lehmann L, Keller L, West S, Roze D (2007) Group selection and kin selection: two concepts but one process. Proc Natl Acad Sci U S A 104:6736–6739

    Article  PubMed  CAS  Google Scholar 

  • Lenz M (1994) Food resources, colony growth and caste development in wood-feeding termites. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, CO, pp 159–209

    Google Scholar 

  • Lenz M, Barrett RA, Williams ER (1985) Reproductive strategies in Cryptotermes: neotenic production in indigenous and ‘tramp’species in Australia (Isoptera: Kalotermitidae). In: Watson J, Okot-Kotber B, Noirot C (eds) Caste differentiation in social insects. Pergamon Press, Oxford, pp 147–163

    Google Scholar 

  • Light SF (1943) The determination of caste of social insects. Q Rev Biol 18:46–63

    Article  Google Scholar 

  • Light SF, Weesner FM (1951) Further studies on the production of supplementary reproductives in Zootermopsis (Isoptera). J Exp Zool 117:397–414

    Article  Google Scholar 

  • Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 47:131

    Article  Google Scholar 

  • Linksvayer TA, Wade MJ (2005) The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q Rev Biol 80:317–336

    Article  PubMed  Google Scholar 

  • Lo N, Tokuda G, Watanabe H et al (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804

    Article  PubMed  CAS  Google Scholar 

  • Lüscher M (1952) Die Produktion und Elimination von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis (Fabr.). Z Vgl Physiol 34:123–141

    Google Scholar 

  • Lüscher M (1964) Die spezifische Wirkung männlicher und weiblicher Ersatzgeschlechtstiere auf die Entstehung von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis (Fabr.). Insectes Soc 11:79–90

    Article  Google Scholar 

  • Lüscher M (1974) Kasten und Kastendifferenzierung bei niederen Termiten. In: Schmidt GH (ed) Sozialpolymorphismus bei Insekten. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 694–739

    Google Scholar 

  • Matthews RW (1991) Evolution of social behavior in sphecid wasps. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 570–602

    Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Belknap Press, Cambridge, MA

    Google Scholar 

  • Michener CD (1975) A taxonomic study of African allodapine bees. Bull Am Mus Nat Hist 155:67–240

    Google Scholar 

  • Michener CD (1985) From solitary to eusocial: need there be a series of intervening species? In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Gustav Fischer, Stuttgart, pp 293–305

    Google Scholar 

  • Michener CD (1990) Reproduction and castes in social halictine bees. In: Engels W (ed) Social insects: an evolutionary approach to castes and reproduction. Springer, Heidelberg, pp 77–121

    Google Scholar 

  • Michener CD, Brothers DJ (1974) Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc Natl Acad Sci U S A 71:671–674

    Article  PubMed  CAS  Google Scholar 

  • Michod RE (1982) The theory of kin selection. Annu Rev Ecol Syst 13:23–55

    Article  Google Scholar 

  • Mill AE (1984) Exploding termites – an unusual defensive behaviour. Entomol Mon Mag 120:179–183

    Google Scholar 

  • Miyata H, Furuichi H, Kitade O (2004) Patterns of neotenic differentiation in a subterranean termite, Reticulitermes speratus (Isoptera: Rhinotermitidae). Entomol Sci 7:309–314

    Article  Google Scholar 

  • Morgan FD (1959) The ecology and external morphology of Stolotermes ruficeps Brauer (Isoptera: Hodotermitidae). Trans R Soc N Z 86:155–195

    Google Scholar 

  • Myles TG (1986) Reproductive soldiers in the Termopsidae (Isoptera). Pan-Pac Entomol 62:293–299

    Google Scholar 

  • Myles TG (1988) Resource inheritance in social evolution from termites to man. In: Slobodchikoff CN (ed) The ecology of social behavior. Academic Press. New York, NY, pp 379–423

    Google Scholar 

  • Nagin R (1972) Caste determination in Neotermes jouteli (Banks). Insectes Soc 19:39–61

    Article  Google Scholar 

  • Nalepa CA (1994) Nourishment and the origin of termite eusociality. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, CO, pp 57–104

    Google Scholar 

  • Nalepa CA, Bandi C (2000) Characterizing the ancestors: paedomorphosis and termite evolution. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 53–75

    Google Scholar 

  • Noirot C (1969) Formation of castes in the higher termites. In: Krishna K, Weesner FM (eds) Biology of termites (vol 1). Academic Press, New York, NY, pp 311–350

    Google Scholar 

  • Noirot C (1985a) Differentiation of reproductives in higher termites. In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Caste differentiation in social insects. Oxford Pergamon, Oxford, pp 177–186

    Google Scholar 

  • Noirot C (1985b) Pathways of caste development in the lower termites. In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Caste Differentiation in Social Insects. Oxford Pergamon, Oxford, 41–58

    Google Scholar 

  • Noirot C (1989) Social structure in termite societies. Ethol Ecol Evol 1:1–17

    Article  Google Scholar 

  • Noirot C (1990) Sexual castes and reproductive strategies in termites. In: Engels W (ed) Social insects: an evolutionary approach to castes and reproduction. Springer, Berlin, pp 5–35

    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 Publishers, Dordrecht, pp 121–140

    Google Scholar 

  • Noirot C, Pasteels JM (1987) Ontogenetic development and evolution of the worker caste in termites. Cell Mol Life Sci 43:851–860

    Article  Google Scholar 

  • Noirot C, Pasteels JM (1988) The worker caste is polyphyletic in termites. Sociobiology 14:15–20

    Google Scholar 

  • Noirot C, Thorne BL (1988) Ergatoid reproductives in Nasutitermes columbicus (Isoptera, Termitidae). J Morphol 195:83–93

    Article  Google Scholar 

  • Nonacs P, Liebert AE, Starks PT (2006) Transactional skew and assured fitness return models fail to predict patterns of cooperation in wasps. Am Nat 167:467–480

    Article  PubMed  Google Scholar 

  • Nonacs P, Reeve HK (1995) The ecology of cooperation in wasps: causes and consequences of alternative reproductive decisions. Ecology 76:953–967

    Article  Google Scholar 

  • O‘Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323–346

    Article  PubMed  Google Scholar 

  • Okasha S (2006) Evolution and the levels of selection. Oxford University Press, Oxford

    Book  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Pamilo P (1991) Evolution of the sterile caste. J Theor Biol 149:75–95

    Article  PubMed  CAS  Google Scholar 

  • Pardi L (1948) Dominance order in Polistes wasps. Physiol Zool 21:1–13

    PubMed  CAS  Google Scholar 

  • Peeters C, Ito F (2001) Colony dispersal and the evolution of queen morphology in social Hymenoptera. Annu Rev Entomol 46:601–630

    Article  PubMed  CAS  Google Scholar 

  • Pellens R, D’Haese CA, Bellés X et al (2007) The evolutionary transition from subsocial to eusocial behaviour in Dictyoptera: phylogenetic evidence for modification of the “shift-in-dependent-care” hypothesis with a new subsocial cockroach. Mol Phylogenet Evol 43:616–626

    Article  PubMed  CAS  Google Scholar 

  • Pen I, Weissing FJ (2000) Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined. Proc R Soc Lond B 267:2411–2418

    Article  Google Scholar 

  • Pereboom JJM, Velthuis HHW, Duchateau MJ (2003) The organisation of larval feeding in bumblebees (Hymenoptera, Apidae) and its significance to caste differentiation. Insectes Soc 50:127–133

    Article  Google Scholar 

  • Poinar GO, Danforth BN (2006) A fossil bee from Early Cretaceous Burmese amber. Science 314:614

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Queller DC (1996) The origin and maintenance of eusociality: the advantage of extended parental care. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps (vol 12). Oxford University Press, Oxford, pp 218–234

    Google Scholar 

  • Queller DC, Strassmann JE (1998) Kin selection and social insects. BioScience 48:165–175

    Article  Google Scholar 

  • Queller DC, Zacchi F, Cervo R et al (2000) Unrelated helpers in a social insect. Nature 405:784–787

    Article  PubMed  CAS  Google Scholar 

  • Ragsdale JE (1999) Reproductive skew theory extended: the effect of resource inheritance on social organization. Evol Ecol Res 1:859–874

    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, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Ann Rev Entomol 51:581–608

    Article  CAS  Google Scholar 

  • Ratnieks FLW, Reeve HK (1991) The evolution of queen-rearing nepotism in social Hymenoptera: effects of discrimination costs in swarming species. J Evol Biol 4:93–115

    Article  Google Scholar 

  • Ratnieks FLW, Wenseleers T (2008) Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol Evol 23:45–52

    Article  PubMed  Google Scholar 

  • Reeve HK (1991) Polistes. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 99–148

    Google Scholar 

  • Reeve HK, Hölldobler B (2007) The emergence of a superorganism through intergroup competition. Proc Natl Acad Sci U S A 104:9736

    Article  PubMed  CAS  Google Scholar 

  • Reeve HK, Keller L (2001) Tests of reproductive-skew models in social insects. Annu Rev Entomol 46:347–385

    Article  PubMed  CAS  Google Scholar 

  • Reeve HK, Peters JM, Nonacs P, Starks PT (1998) Dispersal of first workers in social wasps: causes and implications of an alternative reproductive strategy. Proc Natl Acad Sci U S A 95:13737–13742

    Article  PubMed  CAS  Google Scholar 

  • Reeve HK, Ratnieks F (1993) Queen-queen conflict in polygynous societies: mutual tolerance and reproductive skew. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 45–85

    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  Google Scholar 

  • Reuter M, Keller L (2001) Sex ratio conflict and worker production in eusocial Hymenoptera. Am Nat 158:166–177

    Article  PubMed  CAS  Google Scholar 

  • Richards MH, French D, Paxton RJ (2005) It’s good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee. Mol Ecol 14:4123–4133

    Article  PubMed  Google Scholar 

  • Roisin Y (1988) Morphology, development and evolutionary significance of the working stages in the caste system of Prorhinotermes (Insecta, Isoptera). Zoomorphology 107:339–347

    Article  Google Scholar 

  • Roisin Y (1994) Intragroup conflicts and the evolution of sterile castes in termites. Am Nat 143:751–765

    Article  Google Scholar 

  • Roisin Y (1999) Philopatric reproduction, a prime mover in the evolution of termite sociality? Insectes Soc 46:297–305

    Article  Google Scholar 

  • Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 95–119

    Google Scholar 

  • Roisin Y, Pasteels JM (1991) Polymorphism in the giant cocoa termite, Neotermes papua (Desneux). Insectes Soc 38:263–272

    Article  Google Scholar 

  • Röseler PF (1985) Endocrine basis of dominance and reproduction in polistine paper wasps. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Sinauer, Sunderland, MA, pp 259–272

    Google Scholar 

  • Röseler PF (1991) Reproductive competition during colony establishment. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 309–335

    Google Scholar 

  • Rosengaus RB, Lefebvre ML, Carlock DM, Traniello JFA (2000) Socially transmitted disease in adult reproductive pairs of the dampwood termite Zootermopsis angusticollis. Ethol Ecol Evol 12:419–433

    Article  Google Scholar 

  • Roubaud E (1916) Recherches biologiques sur les guëpes solitaires et sociales d‘Afrique. La genèse de la vie sociale et l’évolution de l’instinct maternel chez les vespides. Ann Sc Nat Zool 1:1–160

    Google Scholar 

  • Sanetra M, Crozier RH (2002) Daughters inherit colonies from mothers in the ‘living-fossil’ ant Nothomyrmecia macrops. Naturwissenschaften 89:71–74

    Article  PubMed  CAS  Google Scholar 

  • Scharf ME, Ratliff CR, Wu-Scharf D et al (2005) Effects of juvenile hormone III on Reticulitermes flavipes: changes in hemolymph protein composition and gene expression. Insect Biochem Mol Biol 35:207–215

    Article  PubMed  CAS  Google Scholar 

  • Schwarz MP, Richards MH, Danforth BN (2006) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu Rev Entomol 52:127–150

    Article  CAS  Google Scholar 

  • Seeley TD (1995) The wisdom of the hive: the social physiology of Honey Bee colonies. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Seger J (1983) Conditional relatedness, recombination, and the chromosome number of insects. In: Rhodin AGJ, Miyata K (eds) Advances in herpetology and evolutionary biology. Essays in honor of Ernst E. Mayr. Harvard University Press, Cambridge, MA, pp 596–612

    Google Scholar 

  • Seger J (1991) Cooperation and conflict in social insects. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific Publications, Oxford, pp 338–373

    Google Scholar 

  • Sen R, Gadagkar R (2005) Males of the social wasp Ropalidia marginata can feed larvae, given an opportunity. Anim Behav 71:345–350

    Article  Google Scholar 

  • Sewell JJ, Watson JAL (1981) Developmental pathwavs in Australian species of Kalotermes Hagen (Isoptera). Sociobiology 6:243–324

    Google Scholar 

  • Shellman-Reeve JS (1997) The spectrum of eusociality in termites. In: Choe J, Crespi B (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, UK, pp 52–93

    Google Scholar 

  • Shellman-Reeve JS (2001) Genetic relatedness and partner preference in a monogamous, wood-dwelling termite. Anim Behav 61:869–876

    Article  Google Scholar 

  • Sherman PW (1979) Insect chromosome numbers and eusociality. Am Nat 113:925–935

    Article  Google Scholar 

  • Sherman PW, Jarvis JUM, Alexander RD (1991) Biology of the Naked Mole-Rat. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409

    Article  Google Scholar 

  • Smith AR, Wcislo WT, O’Donnell S (2003) Assured fitness returns favor sociality in a mass-provisioning sweat bee, Megalopta genalis (Hymenoptera: Halictidae). Behav Ecol Sociobiol 54:22–29

    Article  Google Scholar 

  • Smith AR, Wcislo WT, O’Donnell S (2007) Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae). Behav Ecol Sociobiol 61:1111–1120

    Article  Google Scholar 

  • Springhetti A (1969) II controllo sociale della differenziazione degli alati In Kalotermes flavicollis (Isoptera). Ann Univ Ferrara (Sez 3) 3:73–96

    Google Scholar 

  • Starr CK (1985) Enabling mechanisms in the origin of sociality in the Hymenoptera – the sting’s the thing. Ann Entomol Soc Am 78:836–840

    Google Scholar 

  • Starr CK (1989) In reply, is the sting the thing? Ann Entomol Soc Am 82:6–8

    Google Scholar 

  • Starr CK (1990) Holding the fort: colony defense in some primitively social wasps. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, NY, pp 421–463

    Google Scholar 

  • Starr CK (1991) The nest as the locus of social life. In: Ross KG, Matthews RW (eds) The social biology of wasps. Comstock Publishing Associates. Ithaca, New York, NY, pp 520–539

    Google Scholar 

  • Strassmann J (2001) The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc 48:1–13

    Article  Google Scholar 

  • Strohm E, Liebig J (2008) Why are so many bees but so few digger wasps social? The effect of provisioning mode and helper efficiency on the distribution of sociality among the Apoidea. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 109–128

    Chapter  Google Scholar 

  • Templeton AR (1979) Chromosome number, quantitative genetics and eusociality. Am Nat 113:937–941

    Article  Google Scholar 

  • Thompson GJ, Hebert PDN (1998) Population genetic structure of the neotropical termite Nasutitermes nigriceps (Isoptera: Termitidae). Heredity 80:48–55

    Article  Google Scholar 

  • Thompson GJ, Kitade O, Lo N et al (2000) Phylogenetic evidence for a single, ancestral origin of a ‘true’ worker caste in termites. J Evol Biol 13:869–881

    Article  Google Scholar 

  • Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28:27–54

    Article  Google Scholar 

  • Thorne BL, Breisch NL, Haverty MI (2002) Longevity of kings and queens and first time of production of fertile progeny in dampwood termite (Isoptera; Termopsidae; Zootermopsis) colonies with different reproductive structures. J Anim Ecol 71:1030–1041

    Article  Google Scholar 

  • Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proc Natl Acad Sci U S A 100:12808–12813

    Article  PubMed  CAS  Google Scholar 

  • Thorne BL, Carpenter JM (1992) Phylogeny of the Dictyoptera. Syst Entomol 17:253–268

    Article  Google Scholar 

  • Thorne BL, Grimaldi DA, Krishna K (2000) Early fossil history of the termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 77–93

    Google Scholar 

  • Thorne BL, Lenz M (2001) Population and colony structure of Stolotermes inopinus and S. ruficeps (Isoptera: Stolotermitinae) in New Zealand. N Z Entomol 24:63–70

    Article  Google Scholar 

  • Thorne BL, Noirot C (1982) Ergatoid reproductives in Nasutitermes corniger (Motschulsky) (Isoptera: Termitidae). Int J Insect Morphol Embryol 11:213–226

    Article  Google Scholar 

  • Thorne BL, Traniello JFA (2003) Comparative social biology of basal taxa of ants and termites. Annu Rev Entomol 48:283–306

    Article  PubMed  CAS  Google Scholar 

  • Toth AL, Varala K, Newman TC et al (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tschinkel WR (1988) Colony growth and the ontogeny of worker polymorphism in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 22:103–115

    Article  Google Scholar 

  • Vargo EL, Passera L (1991) Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr). Behav Ecol Sociobiol 28:161–169

    Article  Google Scholar 

  • Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682

    Article  Google Scholar 

  • Wade MJ (2001) Maternal effect genes and the evolution of sociality in haplo-diploid organisms. Evolution 55:453–458

    Article  PubMed  CAS  Google Scholar 

  • Waller DA, LaFage JP (1987) Nutritional ecology of termites. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, NY, pp 487–532

    Google Scholar 

  • Waloff N (1957) The effect of the number of queens of the ant Lasius flavus (Fab.) (Hym., Formicidae) on their survival and on the rate of development of the first brood. Insectes Soc 4:391–408

    Article  Google Scholar 

  • Ward PS (1983) Genetic relatedness and colony organization in a species complex of ponerine ants. Behav Ecol Sociobiol 12:285–299

    Article  Google Scholar 

  • Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • West-Eberhard MJ (1978) Polygyny and the evolution of social behavior in wasps. J Kansas Entomol Soc 51:832–856

    Google Scholar 

  • West-Eberhard MJ (1987) The epigenetical origins of insect sociality. In: Eder J, Rembold H (eds) Chemistry and biology of social insects. Verlag J Peperny, München, pp 369–372

    Google Scholar 

  • West-Eberhard MJ (1996) Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, New York, NY, pp 290–317

    Google Scholar 

  • Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13–34

    Article  Google Scholar 

  • Wheeler DE (1991) The developmental basis of worker caste polymorphism in ants. Am Nat 138:1218–1238

    Article  Google Scholar 

  • Wilfert L, Gadau J, Schmid-Hempel P (2007) Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98:189–197

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495

    Article  PubMed  CAS  Google Scholar 

  • Wilson EO (1987) The earliest known ants: an analysis of the Cretaceous species and an inference concerning their social organization. Paleobiology 13:44–53

    Google Scholar 

  • Wilson EO (2005) Kin selection as the key to altruism: its rise and fall. Soc Res 72:1–8

    Article  Google Scholar 

  • Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. BioScience 58:17–25

    Article  Google Scholar 

  • Wilson EO, Hölldobler B (2005a) Eusociality: origin and consequences. Proc Natl Acad Sci U S A 102:13367–13371

    Article  PubMed  CAS  Google Scholar 

  • Wilson EO, Hölldobler B (2005b) The rise of the ants: a phylogenetic and ecological explanation. Proc Natl Acad Sci U S A 102:7411–7414

    Article  PubMed  CAS  Google Scholar 

  • Wilson DS, Wilson EO (2007) Rethinking the theoretical foundation of sociobiology. Q Rev Biol 82:327–348

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Yanega D (1988) Social plasticity and early-diapausing females in a primitively social bee. Proc Natl Acad Sci U S A 85:4374–4377

    Article  PubMed  CAS  Google Scholar 

  • Zhou X, Oi FM, Scharf ME (2006) Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc Natl Acad Sci U S A 103:4499–4504

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman RB (1983) Sibling manipulation and indirect fitness in termites. Behav Ecol Sociobiol 12:143–145

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenneth J. Howard .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Howard, K.J., Thorne, B.L. (2010). Eusocial Evolution in Termites and Hymenoptera. In: Bignell, D., Roisin, Y., Lo, N. (eds) Biology of Termites: a Modern Synthesis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3977-4_5

Download citation

Publish with us

Policies and ethics