Insectes Sociaux

, Volume 63, Issue 1, pp 5–14 | Cite as

Social evolution and casteless societies: needs for new terminology and a new evolutionary focus

Review Article

Abstract

There has been considerable debate surrounding the evolution of eusociality, which has recently increased in vigor with regard to what actually constitutes eusociality. Surprisingly, there has been little discussion on terminologies for describing social systems that are more-or-less egalitarian, yet such societies form an obvious contrast to eusociality, and transitions between these two forms of social organization appear to be common. We argue that current terminologies and methods for dealing with non-hierarchical societies are not well suited for such comparative approaches to social evolution. We outline three problems for comparative approaches (identifying egalitarianism, implied egalitarianism and taxon-specific terminology) and propose two solutions. The first solution is a re-sampling method to assess investment asymmetries, and the second is the introduction of the term “casteless” to encompass forms of social organization where there is no lifetime commitment to queen-like or worker-like roles, but where skew in reproduction or alloparental tasks may nevertheless be apparent at any one time. Our suggested terminology avoids the implied egalitarian nature behind the terms communal and quasisocial, which place undue emphasis on specific nesting biologies and which have the potential to impede ‘bottom-up’ comparative studies of social evolution. Such non-eusocial groups provide the best insights for understanding how social behavior evolved and our suggested approaches should enhance future investigations.

Keywords

Social evolution Communal Quasisocial Eusocial Egalitarian Despotic 

Notes

Acknowledgments

We would like to thank S. M. Rehan and two anonymous reviewers for constructive comments on previous versions of this manuscript. This project was funded by grants from the Holsworth Wildlife Research Endowment and the Sir Mark Mitchell Research Foundation to RM Dew.

References

  1. Abbot P, Abe J, Alizon S et al (2011) Inclusive fitness theory and eusociality. Nature 471:E1–E4. doi: 10.1038/nature09831 PubMedCrossRefGoogle Scholar
  2. Aviles L, Harwood G (2012) A quantitative index of sociality and its application to group-living spiders and other social organisms. Ethology 118:1219–1229. doi: 10.1111/eth.12028 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Batra SWT (1966) Nests and social behaviour of halictine bees of India. Indian J Entomol 28:375–393Google Scholar
  4. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440. doi: 10.1146/annurev.ento.46.1.413 PubMedCrossRefGoogle Scholar
  5. Boomsma JJ (2013) Beyond promiscuity: mate-choice commitments in social breeding. Philos T R Soc B 368:20120050. doi: 10.1098/rstb.2012.0050 CrossRefGoogle Scholar
  6. 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. doi: 10.1093/beheco/arp050 CrossRefGoogle Scholar
  7. Buston PM, Reeve HK, Cant MA, Vehrencamp SL, Emlen ST (2007) Reproductive skew and the evolution of group dissolution tactics: a synthesis of concession and restraint models. Anim Behav 74:1643–1654. doi: 10.1016/j.anbehav.2007.03.003 CrossRefGoogle Scholar
  8. Cameron SA (2004) Phylogeny and biology of neotropical orchid bees. Annu Rev Entomol 49:377–404. doi: 10.1146/annurev.ento.49.072103.115855 PubMedCrossRefGoogle Scholar
  9. Cardinal S, Danforth BN (2011) The antiquity and evolutionary history of social behavior in bees. PLoS One 6:e21086. doi: 10.1371/journal.pone.0021086 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Crespi BJ (2009) Social conflict resolution, life history, and the reconstruction of skew. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 480–507CrossRefGoogle Scholar
  11. Crespi BJ, Yanega D (1995) The definition of eusociality. Behav Ecol 6:109–115. doi: 10.1093/beheco/6.1.109 CrossRefGoogle Scholar
  12. da Silva CRB, Stevens MI, Schwarz MP (2015) Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies. Insect Soc. doi: 10.1007/s00040-015-0436-0 Google Scholar
  13. Dalmazzo M, Roig-Alsina A (2015) Social biology of Augochlora (Augochlora) phoemonoe (Hymenoptera, Halictidae) reared in laboratory nests. Insect Soc 62:315–323. doi: 10.1007/s00040-015-0412-8 CrossRefGoogle Scholar
  14. Danforth BN (2002) Evolution of sociality in a primitively eusocial lineage of bees. P Natl Acad Sci USA 99:286–290. doi: 10.1073/pnas.012387999 CrossRefGoogle Scholar
  15. Danforth BN, Eickwort GC (1997) The evolution of social behavior in the augochlorine sweat bees (Hymenoptera: Halictidae) based on a phylogenetic analysis of the genera. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 270–292CrossRefGoogle Scholar
  16. Dew RM, Rehan SM, Tierney SM, Chenoweth LB, Schwarz MP (2012) A single origin of large colony size in allodapine bees suggests a threshold event among 50 million years of evolutionary tinkering. Insect Soc 59:207–214. doi: 10.1007/s00040-011-0206-6 CrossRefGoogle Scholar
  17. Doody JS (2009) Communal egg-laying in reptiles and amphibians: evolutionary patterns and hypotheses. Q Rev Biol 84:229–252. doi: 10.1086/605078 PubMedCrossRefGoogle Scholar
  18. Eickwort GC, Eickwort KR (1971) Aspects of the biology of Costa Rican halictine bees, II. Dialictus umbripennis and adaptations of its caste structure to different climates. J Kansas Entomol Soc 44:343–373Google Scholar
  19. Gardner A (2015) The genetical theory of multilevel selection. J Evol Biol 28:305–319. doi: 10.1111/jeb.12566 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Gardner MG, Pearson SK, Johnston GR, Schwarz MP (2015) Group living in squamate reptiles: a review of evidence for stable aggregations. Biol Rev. doi: 10.1111/brv.12201 PubMedGoogle Scholar
  21. Gibbs J, Brady SG, Kanda K, Danforth BN (2012) Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Mol Phylogenet Evol 65:926–939. doi: 10.1016/j.ympev.2012.08.013 PubMedCrossRefGoogle Scholar
  22. Giovanetti M, Jacobi B (2013) Influence of temperature and body size on activities of a social wasp, Cerceris rubida (Hymenoptera Crabronidae). Ethol Ecol Evol 25:319–329. doi: 10.1080/03949370.2013.808704 CrossRefGoogle Scholar
  23. Gorelick R, Bertram SM, Killeen PR, Fewell JH (2004) Normalized mutual entropy in biology: quantifying division of labor. Am Nat 164:677–682. doi: 10.1086/424968 PubMedCrossRefGoogle Scholar
  24. Hamilton WD (1964a) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16. doi: 10.1016/0022-5193(64)90038-4 PubMedCrossRefGoogle Scholar
  25. Hamilton WD (1964b) The genetical evolution of social behaviour. II. J Theor Biol 7:17–52. doi: 10.1016/0022-5193(64)90039-6 PubMedCrossRefGoogle Scholar
  26. Hogendoorn K, Velthuis HHW (1999) Task allocation and reproductive skew in social mass provisioning carpenter bees in relation to age and size. Insect Soc 46:198–207. doi: 10.1007/s000400050135 CrossRefGoogle Scholar
  27. Holman L (2014) Conditional helping and evolutionary transitions to eusociality and cooperative breeding. Behav Ecol 25:1173–1182. doi: 10.1086/674052 CrossRefGoogle Scholar
  28. Hu Z, Zhao X, Li Y, Liu X, Zhang Q (2012) Maternal care in the parasitoid Sclerodermus harmandi (Hymenoptera: Bethylidae). PLoS One 7:351246. doi: 10.1371/journal.pone.0051246 Google Scholar
  29. Johnstone RA (2000) Models of reproductive skew: a review and synthesis. Ethology 106:5–26. doi: 10.1046/j.1439-0310.2000.00529.x CrossRefGoogle Scholar
  30. Kapheim KM, Pan H, Li C et al (2015) Genomic signatures of evolutionary transitions from solitary to group living. Science. doi: 10.1126/science.aaa4788 PubMedGoogle Scholar
  31. Knerer G, Schwarz M (1976) Halictine social evolution: the Australian enigma. Science 194:445–448. doi: 10.1126/science.194.4263.445 PubMedCrossRefGoogle Scholar
  32. Knerer G, Schwarz M (1978) Beobachtungen an australischen Furchenbienen (Hymenoptera; Halictinae). Zool Anz 200:321–333Google Scholar
  33. Kocher SD, Paxton RJ (2014) Comparative methods offer powerful insights into social evolution in bees. Apidologie 45:289–305. doi: 10.1007/s13592-014-0268-3 CrossRefGoogle Scholar
  34. Kocher SD, Pellissier L, Veller C, Purcell J, Nowak MA, Chapuisat M, Pierce NE (2014) Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution. P R Soc B 281:20140627. doi: 10.1098/rspb.2014.0627 CrossRefGoogle Scholar
  35. Kukuk PF, Ward SA, Jozwiak A (1998) Mutualistic benefits generate an unequal distribution of risky activities among unrelated group members. Naturwissenschaften 85:445–449. doi: 10.1007/s001140050528 CrossRefGoogle Scholar
  36. Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 47:131–159CrossRefGoogle Scholar
  37. Michener CD (1969) Comparative social behavior of bees. Annu Rev Entomol 14:299–342. doi: 10.1146/annurev.en.14.010169.001503 CrossRefGoogle Scholar
  38. Michener CD (1971) Biologies of African allodapine bees. Bull Am Mus Nat Hist 145:219–302Google Scholar
  39. Michener CD (1974) The social behavior of the bees. Harvard University Press, CambridgeGoogle Scholar
  40. Michener CD (1985) From solitary to eusocial: need there be a series of intervening species? In: Holldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Gustav Fischer Verlag, Stuttgart, pp 293–305Google Scholar
  41. Michener CD (1990) Reproduction and castes in social halictine bees. In: Engels W (ed) Social insects. An evolutionary approach to castes and reproduction. Springer, New York, pp 77–122Google Scholar
  42. Mueller UG, Wolf-Mueller B (1993) A method for estimating the age of bees: age-dependent wing wear and coloration in the woolcarder bee Anthidium manicatum. J Insect Behav 6:529–537. doi: 10.1007/BF01049530 CrossRefGoogle Scholar
  43. Nonacs P, Hager R (2011) The past, present and future of reproductive skew theory and experiments. Biol Rev 86:271–298. doi: 10.1111/j.1469-185X.2010.00144.x PubMedCrossRefGoogle Scholar
  44. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062. doi: 10.1038/nature09205 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167:808–825. doi: 10.1086/503444 PubMedCrossRefGoogle Scholar
  46. Pamilo P, Crozier RH (1996) Reproductive skew simplified. OIKOS 75:533–535. doi: 10.2307/3545895 CrossRefGoogle Scholar
  47. Paxton RJ, Thorén PA, Tengö J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519. doi: 10.1046/j.1365-294X.1996.00117.x PubMedCrossRefGoogle Scholar
  48. Plateaux-Quénu C (2008) Subsociality in halictine bees. Insect Soc 55:335-346. doi: 10.1007/s00040-008-1028-z CrossRefGoogle Scholar
  49. Purcell J (2011) Geographic patterns in the distribution of social systems in terrestrial arthropods. Biol Rev 86:475–491. doi: 10.1111/j.1469-185X.2010.00156.x PubMedCrossRefGoogle Scholar
  50. Quiñones AE, Wcislo WT (2015) Cryptic extended brood care in the facultatively eusocial sweat bee Megalopta genalis. Insect Soc. doi: 10.1007/s00040-015-0409-3 Google Scholar
  51. Rautiala P, Helantera H, Puurtinen M (2014) Unmatedness promotes the evolution of helping more in diplodiploids than in haplodiploids. Am Nat 184:318–325. doi: 10.1086/677309 PubMedCrossRefGoogle Scholar
  52. Reeve HK, Keller L (2001) Tests of reproductive-skew models in social insects. Annu Rev Entomol 46:347–385. doi: 10.1146/annurev.ento.46.1.347 PubMedCrossRefGoogle Scholar
  53. Rehan SM, Richards MH (2010) Nesting biology and subsociality in Ceratina calcarata (Hymanoptera: Apidae). Can Entomol 142:65–74. doi: 10.4039/n09-056 CrossRefGoogle Scholar
  54. Rehan SM, Toth AL (2015) Climbing the social ladder: the molecular evolution of sociality. TREE Genet Genomes. doi: 10.1016/j.tree.2015.05.004 Google Scholar
  55. Rehan SM, Richards MH, Schwarz MP (2009) Evidence of social nesting in the Ceratina of Borneo (Hymenoptera: Apidae). J Kansas Entomol Soc 82:194–209. doi: 10.2317/JKES809.22.1 CrossRefGoogle Scholar
  56. Rehan SM, Schwarz MP, Richards MH (2011) Fitness consequences of ecological constraints and implications for the evolution of sociality in an incipiently social bee. Biol J Linn Soc 103:57–67. doi: 10.1111/j.1095-8312.2011.01642.x CrossRefGoogle Scholar
  57. Rehan SM, Leys R, Schwarz MP (2012) A mid-cretaceous origin of sociality in xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality. PLoS One 7:e34690. doi: 10.1371/journal.pone.0034690 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Sakagami SF, Maeta Y (1984) Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera, Xylocopinae). J Kansas Entomol Soc 57:639–656Google Scholar
  59. Schwarz MP (1986) Persistent multi-female nests in an Australian allodapine bee, Exoneura bicolor (Hymenoptera, Anthophoridae). Insect Soc 33:258–277. doi: 10.1007/BF02224245 CrossRefGoogle Scholar
  60. Schwarz MP, Tierney SM, Zammit J, Schwarz PM, Fuller S (2005) Brood provisioning and colony composition of a Malagasy species of Halterapis: implications for social evolution in the allodapine bees. Ann Entomol Soc Am 98:126–133CrossRefGoogle Scholar
  61. Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu Rev Entomol 52:127–150. doi: 10.1146/annurev.ento.51.110104.150950 PubMedCrossRefGoogle Scholar
  62. Schwarz MP, Tierney SM, Rehan SM, Chenoweth L, Cooper SJB (2011) The evolution of eusociality in allodapine bees: workers began by waiting. Biol Lett 7:277–280. doi: 10.1098/rsbl.2010.0757 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Spessa A, Schwarz MP, Adams M (2000) Sociality in Amphylaeus morosus (Hymenoptera: Colletidae: Hylaeinae). Ann Entomol Soc Am 93:684–692CrossRefGoogle Scholar
  64. Stark RE, Hefetz A, Gerling D, Velthuis HHW (1990) Reproductive competition involving oophagy in the socially nesting bee Xylocopa sulcatipes. Naturwissenschaften 77:38–40. doi: 10.1007/BF01131797 CrossRefGoogle Scholar
  65. Tang X, Meng L, Kapranas A, Xu F, Hardy ICW, Li B (2014) Mutually beneficial host exploitation and ultra-biased sex ratios in quasisocial parasitoids. Nature 5:4942. doi: 10.1038/ncomms5942 Google Scholar
  66. Tierney SM, Schwarz MP (2009) Reproductive hierarchies in the African allodapine bee Allodapula dichroa (Apidae: Xylocopinae) and ancestral forms of sociality. Biol J Linn Soc 97:520–530. doi: 10.1111/j.1095-8312.2009.01236.x CrossRefGoogle Scholar
  67. Tierney SM, Gonzales-Ojeda T, Wcislo WT (2008a) Nesting biology and social behavior of two Xenochlora bees (Hymenoptera: Halictidae: Augochlorini) from Perú. J Kansas Entomol Soc 81:61–72. doi: 10.2317/JKES-704.24.1 CrossRefGoogle Scholar
  68. Tierney SM, Smith JA, Chenoweth L, Schwarz MP (2008b) Phylogenetics of allodapine bees: a review of social evolution, parasitism and biogeography. Apidologie 39:3–15. doi: 10.1051/apido:2007045 CrossRefGoogle Scholar
  69. Tierney SM, Fischer CB, Rehan SM, Kapheim KM, Wcislo WT (2013) Frequency of social nesting in the sweat bee Megalopta genalis (Halictidae) does not vary across a rainfall gradient, despite disparity in brood production and body size. Insect Soc 60:163–172. doi: 10.1007/s00040-012-0280-4 CrossRefGoogle Scholar
  70. Vehrencamp SL (1979) The roles of individual, kin, and group selection in the evolution of sociality. In: Marler P, Vandenbergh JG (eds) Handbook of behavioral neurobiology, vol 3. Plenum, New York, pp 351–394Google Scholar
  71. Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682. doi: 10.1016/S0003-3472(83)80222-X CrossRefGoogle Scholar
  72. Ward SA, Kukuk PF (1998) Context-dependent behavior and the benefits of communal nesting. Am Nat 152:249–263. doi: 10.1086/286165 PubMedCrossRefGoogle Scholar
  73. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  74. Wheeler WM (1928) The social insects: their origin and evolution. Kegan Paul and Co. Ltd, LondonGoogle Scholar
  75. Willie A, Orozco E (1970) The life cycle and behavior of the social bee Lasioglossum (Dialictus) umbripenne (Hymenoptera: Halictidae). Rev Biol Trop 17:199–245Google Scholar
  76. Wilson EO (1971) The insect societies. Belknap Press, CambridgeGoogle Scholar
  77. Wilson EO (1975) Sociobiology. Belknap Press, CambridgeGoogle Scholar
  78. Woodard SH, Fischman BJ, Venkat A, Hudson ME, Varala K, Cameron SA, Clark AG, Robinson GE (2011) Genes involved in convergent evolution of eusociality in bees. P Natl Acad Sci USA. doi: 10.1073/pnas.1103457108 Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2015

Authors and Affiliations

  1. 1.School of Biological SciencesFlinders UniversityAdelaideAustralia
  2. 2.School of Biological SciencesThe University of AdelaideAdelaideAustralia

Personalised recommendations