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Insectes Sociaux

, Volume 63, Issue 1, pp 67–78 | Cite as

Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies

  • C. R. B. da Silva
  • M. I. Stevens
  • M. P. Schwarz
Research Article

Abstract

Communal behaviour is a form of social behaviour where two or more females nest together and have no reproductive hierarchies. Communal behaviour has often been regarded as an evolutionary ‘stepping stone’ to more complex forms of sociality involving castes, as well as a social form derived from solitary behaviour with no further evolution towards eusociality. However, recent phylogenetic studies on halictine bees suggest that some instances of communal behaviour are derived from eusociality. Here, we describe social nesting in an allodapine bee, Braunsapis puangensis, which has been introduced to Fiji from southern Asia. We show that this bee has a casteless form of sociality similar to communal organization, but which has been derived from an ancestrally hierarchical social system. This is likely due to a combination of small benefits for social nesting that rapidly saturate as colonies become larger, along with low costs for dispersal. We suggest that casteless forms of sociality have frequently evolved from hierarchical societies across many insect groups, but the analyses required for recognizing such societies are often undeveloped and hampers comparative approaches. Transitions from hierarchical to casteless societies challenge the notion that eusociality is an evolutionary ‘end point’ and we argue that eusociality can, in some cases, be regarded as an evolutionary step towards egalitarian societies. We also suggest that evolutionary periods involving reproductive hierarchies could select for traits that allow individuals to better assess their social environment and subsequently enable lower reproductive skew.

Keywords

Communal Quasisocial Eusocial Allodapini Casteless societies Reproductive skew 

Notes

Acknowledgments

We thank Marika Tuiwawa, Apatia Liga and Hilda Sakitiwaqa at the University of the South Pacific for providing us with laboratory and field support in Fiji. We also thank Simon Tierney for providing us with the Monte Carlo script used in the program ‘R’ to analyse differences in ovary size and wing wear and Scott Groom for allowing the 2013 collections available for analysis. We also thank Miriam Richards, the three anonymous reviewers, Simon Tierney, Karen Burke da Silva, Jack da Silva and Owen Coffee for helpful comments on earlier versions of this manuscript. Our research was supported by two grants from the Australia Pacific Science Foundation.

Reference

  1. Abbot P, Abe J, Alcock J et al (2011) Inclusive fitness theory and eusociality. Nature 471:E1–E10. doi: 10.1038/nature09831 PubMedCrossRefGoogle Scholar
  2. Almeida EAB, Porto DS (2015) Investigating eusociality in bees while trusting the uncertainty. Sociobiol 61:355–368. doi: 10.13102/sociobiology.v61i4.355-368 Google Scholar
  3. Ash J (1992) Vegetation ecology in Fiji: past, present and future perspectives. Pac Sci 46:111–127Google Scholar
  4. Barretto-Ko P, Danforth BN, Neff JL (1996) Nestmate relatedness in a communal bee, Perdita texana (Hymenoptera: Andrenidae), based on DNA fingerprinting. Evolution 50:276–284. doi: 10.2307/2410799 CrossRefGoogle Scholar
  5. Boomsma JJ, Huszar DB, Pedersen JS (2014) The evolution of multiqueen breeding in eusocial lineages with permanent physically differentiated castes. Anim Behav 92:241–252. doi: 10.1016/j.anbehav.2014.03.005 CrossRefGoogle Scholar
  6. Brady SG, Sipes SD, Pearson A, Danforth BN (2006) Recent and simultaneous origins of eusociality in halictine bees. Proc R Soc B 31:293–305. doi: 10.1098/rspb.2006.3496 Google Scholar
  7. Bull NJ, Schwarz MP (2001) Brood insurance via protogyny: a source of female biased sex allocation. Proc R Soc B 268:1869–1874. doi: 10.1098/rspb.2001.1687 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 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
  9. 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, New York, pp 480–507CrossRefGoogle Scholar
  10. Garófalo CA, Camillo E, Augusto SC, Jesus BMV, Serra JC (1998) Nest structure and communal nesting in Euglossa (Glossura) annectans Dressler (Hymenoptera, Apidae, Euglossini). Rev Bras Zool 15:589–596. doi: 10.1590/S0101-81751998000300003 CrossRefGoogle Scholar
  11. Cameron SA (2004) Phylogeny and biology of neotropical orchid bees (Euglossini). Annu Rev Entomol 49:377–404. doi: 10.1146/annurev.ento.49.072103.115855 PubMedCrossRefGoogle Scholar
  12. 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
  13. Chenoweth LB, Tierney TM, Smith JA, Cooper SJB, Schwarz MP (2007) Social complexity in bees is not sufficient to explain lack of reversions to solitary living over long time scales. BMC Evol Biol 7:246–255. doi: 10.1186/1471-2148-7-246 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Clarke FM, Faulkes CG (2001) Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim Behav 61:311–324. doi: 10.1006/anbe.2000.1573 CrossRefGoogle Scholar
  15. Cocom Pech ME, May-Itzá WdJ, Medina Medina LA, Quezada-Euán JJG (2008) Sociality in Euglossa (Euglossa) viridissima Friese (Hymenoptera, Apidae, Euglossini). Insect Soc 55:428–433. doi: 10.1007/s00040-008-1023-4 CrossRefGoogle Scholar
  16. da Silva CRB, Groom SVC, Stevens MI, Schwarz MP (2015) Current status of the introduced allodapine bee Braunsapis puangensis (Hymenoptera: Apidae) in Fiji. Aust Entomol. doi: 10.1111/aen.12149 Google Scholar
  17. Danforth BN (1999) Phylogeny of the bee genus Lasioglossum (Hymenoptera: Halictidae) based on mitochondrial COI sequence data. Syst Entomol 24:377–393. doi: 10.1046/j.1365-3113.1999.00087.x CrossRefGoogle Scholar
  18. Danforth BN (2002) Evolution of sociality in a primitively social lineage of bees. PNAS 99:286–290. doi: 10.1073/pnas.012387999 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Danforth BN, Ji S (2001) Australian Lasioglossum + Homalictus form a monophyletic group: resolving the “Australian Enigma”. Syst Biol 50:268–283. doi: 10.1093/sysbio/50.2.268 PubMedCrossRefGoogle Scholar
  20. Dew RM, Tierney SM, Rehan SM, Chenoweth LB, Schwarz MP (2012) Sociality in allodapine bees: a single origin of large colony size 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
  21. Dew RM, Tierney SM, Schwarz MP (2015) Social evolution and casteless societies: needs for new terminology and a new evolutionary focus. Insect Soc. doi: 10.1007/s00040-015-0435-1 Google Scholar
  22. Fu F, Kocher SD, Nowak MA (2015) The risk-return trade-off between solitary and eusocial reproduction. Ecol Lett 18:74–84. doi: 10.1111/ele.12392 PubMedCrossRefGoogle Scholar
  23. Gibbs J, Brady SG, 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
  24. Hamilton WD (1964) The genetical evolution of social behaviour I. J Theo Biol 7:1–16. doi: 10.1016/0022-5193(64)90038-4 CrossRefGoogle Scholar
  25. Harradine SL, Gardner MG, Schwarz MP (2012) Kinship in a social bee mediates ovarian differentiation and has implications for reproductive skew theories. Anim Behav 84:611–618. doi: 10.1016/j.anbehav.2012.06.016 CrossRefGoogle Scholar
  26. Hogendoorn K, Watiniasih NL, Schwarz MP (2001) Extended alloparental care in the almost solitary bee Exonerella eremophila (Hymenoptera: Apidae). Behav Ecol Sociobiol 50:275–282. doi: 10.1007/s002650100357 CrossRefGoogle Scholar
  27. Jarvis J (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573. doi: 10.1126/science.7209555 PubMedCrossRefGoogle Scholar
  28. Joyce NC, Schwarz MP (2006) Sociality in the Australian allodapine bee Brevineura elongata: small colony sizes despite large benefits to group living. J Insect Behav 19:45–61. doi: 10.1007/s10905-005-9004-1 CrossRefGoogle Scholar
  29. Joyce NC, Schwarz MP (2007) Sociality and sex allocation in an Australian allodapine bee Braunsapis protuberans. Aus J Entomol 46:121–128. doi: 10.1111/j.1440-6055.2007.00590.x CrossRefGoogle Scholar
  30. Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102. doi: 10.1016/0169-5347(94)90204-6 PubMedCrossRefGoogle Scholar
  31. Knerer G, Schwarz MP (1976) Halictine social evolution: the Australian enigma. Science 195:445–448. doi: 10.1126/science.194.4263.445 CrossRefGoogle Scholar
  32. Knerer G, Schwarz MP (1978) Beobachtungen an australischen furchenbienen (Hymenoptera: Halictidae). 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. Proc R Soc B 281:20140627. doi: 10.1098/rspb.2014.0627 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Kranz BD, Schwarz MP, Mound MA, Crespi BJ (1999) Social biology and sex ratios of the eusocial gall-inducing thrips Kladothrips hamiltoni. Ecol Entomol 24:432–442. doi: 10.1046/j.1365-2311.1999.00207.x CrossRefGoogle Scholar
  36. Kukuk PF (1992) Social interactions and familiarity in a communal Halictine bee Lasioglossum (Chilalictus) hemichalceum. Ethology 91:291–300. doi: 10.1111/j.1439-0310.1992.tb00870.x CrossRefGoogle Scholar
  37. Kukuk PF, Sage GK (1994) Reproductivity and relatedness in a communal halictine bee Lasioglossum (Chilalictus) hemichalceum. Insect Soc 41:443–455. doi: 10.1007/BF01240647 CrossRefGoogle Scholar
  38. 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
  39. Lin N, Michener CD (1972) Evolution of sociality in insects. Quart Rev Biol 47:131–159. doi: 10.1086/407216 CrossRefGoogle Scholar
  40. Melna PA, Schwarz MP (1994) Behavioural specialization in pre-reproductive colonies of the allodapine bee Exoneura bicolour (Hymenoptera: Anthophoridae). Insect Soc 41:1–18. doi: 10.1007/BF01240569 CrossRefGoogle Scholar
  41. Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insect Soc 11:317–342. doi:10.1007BF02227433Google Scholar
  42. Michener CD (1969) Comparative social behavior of bees. Annu Rev Entomol 14:299–342. doi: 10.1146/annurev.en.14.010169.001503 CrossRefGoogle Scholar
  43. Michener CD (1985) From solitary to eusocial: need there to be a series of intervening species? Experimental behavioural ecology and sociobiology. Sinaeur Press, Sunderland, pp 293–305Google Scholar
  44. Michener CD (2007) The bees of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  45. Nalepa C (2012) Wing wear is a poor estimate of age in Cerceris fumipennis (Hymenoptera, Crabronidae). J Hymenopt Res 24:43–46. doi: 10.3897/JHR.24.2091 CrossRefGoogle Scholar
  46. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062. doi: 10.1038/nature09205 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Packer L (1998) A phylogenetic analysis of western European species of the Lasioglossum leucozonium species-group (Hymenoptera: Halictidae): sociobiological and taxonomic implications. Can J Zool 76:11611–11621. doi: 10.1139/z98-102 CrossRefGoogle Scholar
  48. 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
  49. Powell S, Franks NR (2005) Caste evolution and ecology: a special worker for a novel prey. Proc R Soc B 272:2173–2180. doi: 10.1098/rspb.2005.3196 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Queller DC, Strassmann JE (1998) Kin selection and social insects. BioScience 48:165–175. doi: 10.2307/1313262 CrossRefGoogle Scholar
  51. 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
  52. Rehan SM, Leys R, Schwarz MP (2012) 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: 10.137/journal.pone.0034690 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Richards MH, von Wettberg EJ, Rutgers AC (2003) A novel social polymorphism in a primitively eusocial bee. PNAS 100:7175–7180. doi: 10.1073/pnas.1030738100 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Rozen JG, McGinley RJ (1976) Biology of the bee genus Conanthalictus (Halictidae, Dufoureinae). Am Mus Novit 2602:1–6Google Scholar
  55. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/
  56. Schwarz MP (1986) Persistent multi-female nests in an Australian allodapine bee Exoneura bicolor. Insect Soc 33:258–277. doi: 10.1007/BF02224245 CrossRefGoogle Scholar
  57. Schwarz MP (1987) Intra-colony relatedness and sociality in the allodapine bee Exoneura bicolor. Behav Ecol Sociobiol 21:387–392. doi: 10.1007/BF00299933 CrossRefGoogle Scholar
  58. Schwarz MP (1988) Intra-specific mutualism and kin-association of cofoundresses in allodapine bees (Hymenoptera, Anthophoridae). Monit Zool Ital 22:245–254. doi: 10.1080/00269786.1988.10736556 Google Scholar
  59. Schwarz MP (1994) Female-biased sex ratios in a facultatively social bee and their implications for social evolution. Evolution 48:1684–1697. doi: 10.2307/2410257 CrossRefGoogle Scholar
  60. Schwarz MP, Lowe RM, Lefevere KS (1996) Kin association in the allodapine bee Exoneura richardsoni Rayment (Hymenoptera: Apidae). Aus J Entomol 35:65–71. doi: 10.1111/j.1440-6055.1996.tb01363.x CrossRefGoogle Scholar
  61. 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 (Hymenoptera: Apidae: Xylocopinae). Annals Ent Soc Amer 98:126–133. doi: 10.1603/0013-8746(2005) 098[0126:BPACCO]2.0.CO;2 CrossRefGoogle Scholar
  62. 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
  63. Schwarz MP, Tierney SM, Rehan SM, Chenoweth LB, Cooper SJB (2011) Evolution of eusociality in allodapine bees: workers began by waiting. Biol Lett 7:277–280. doi: 10.1098/rsbl.2010.0757 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Shibao H (1998) Social structure and the defensive role of soldiers in a eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididea): a test of the defence-optimization hypothesis. Res Pop Ecol 40(325–333):1007. doi:/BF02763464Google Scholar
  65. Spessa A, Schwarz MP, Adams M (2000) Sociality in Amphylaeus morosus (Hymenoptera: Colletidae: Hylaeinae). Ann Entomol Soc Am 93:684–692. doi: 10.1603/0013-8746(2000)093[0684:SIAMHC]2.0.CO;2 CrossRefGoogle Scholar
  66. Stevens MI, Hogendoorn K, Schwarz MP (2007) Evolution of sociality by natural selection on variances in reproductive fitness: evidence from a social bee. BMC Evol Biol 7:153–162. doi: 10.1186/1471-2148-70153 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Szathmáry E, Smith JM (1995) The major evolutionary transitions. Nature 374:227–232. doi: 10.1038/374227a0 PubMedCrossRefGoogle Scholar
  68. Szathmáry E, Smith JM (1997) From replicators to reproducers: the first major transitions leading to life. J Theo Biol 187:555–571. doi: 10.1006/jtbi.1996.0389 CrossRefGoogle Scholar
  69. Thompson S, Schwarz MP (2006) Cooperative nesting and complex female-biased sex allocation in a tropical allodapine bee. Biol J Linn Soc 89:355–364. doi: 10.1111/j.1095-8312.2006.00679.x CrossRefGoogle Scholar
  70. 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
  71. Tierney SM, Cronin AL, Loussert N, Schwarz MP (2000) The biology of Brevineura froggatti and phylogenetic conservatism in Australian allodapine bees (Apidae, Allodapini). Insect Soc 47:96–97. doi: 10.1007/s000400050016 CrossRefGoogle Scholar
  72. 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
  73. Timmermann K, Kuhlmann M (2008) The biology of a Patellapis (s. str.) species (Hymenoptera: Apoidea: Halictidae): sociality described for the first time in this bee genus. Apidologie 39:189–197. doi: 10.1051/apido:2008003 CrossRefGoogle Scholar
  74. Vogel ME, Kukuk PF (1994) Individual foraging effort in the facultatively social halictid bee Nomia (Austronomia) australica (Smith). J Kans Entomol Soc 67:225–235. doi: 10.1051/apido:2009002 Google Scholar
  75. Ward DF, Wetterer JK (2006) Checklist of the ants of Fiji (Hymenoptera: Formicidae). Bishop Mus Occas Pap 85:23–47Google Scholar
  76. Wcislo WT, Tierney SM (2009) The evolution of communal behaviour in bees and wasps: an alternative to eusociality. In: Gadau J, Fewell J (ed) Organization of insect societies. Harvard University Press, Cambridge, pp 148–169Google Scholar
  77. Wcislo WT, Wille A, Orozco E (1993) Nesting biology of tropical solitary and social sweat bees, Lassioglossum (Dialictus) figueresi Wcislo and L. (D.) aeneiventre (Friese) (Hymeoptera: Halictidae). Insect Soc 40:21–40. doi: 10.1007/BF01338830 CrossRefGoogle Scholar
  78. Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. Ecology Institute, Oldendorf/Luhe (Germany)Google Scholar
  79. Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58:17–25. doi: 10.1641/B580106 CrossRefGoogle Scholar
  80. Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. PNAS 102:13367–13371. doi: 10.1073/pnas.0505858102 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Zammit J, Hogendoorn K, Schwarz MP (2008) Strong constraints to independent nesting in a facultatively social bee: quantifying the effects of enemies-at-the-nest. Insect Soc 55:74–78. doi: 10.1007/s00040-007-0972-3 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • C. R. B. da Silva
    • 1
  • M. I. Stevens
    • 2
    • 3
  • M. P. Schwarz
    • 1
  1. 1.Biological SciencesFlinders UniversityAdelaideAustralia
  2. 2.South Australian MuseumAdelaideAustralia
  3. 3.School of Pharmacy and Medical SciencesUniversity of South AustraliaAdelaideAustralia

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