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Cofoundress relatedness and group productivity in colonies of social Dunatothrips (Insecta: Thysanoptera) on Australian Acacia

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Abstract

Facultative joint colony founding by social insects provides opportunities to analyze the roles of genetic and ecological factors in the evolution of cooperation. Although cooperative nesting is observed in range of social insect taxa, the most detailed studies of this behavior have been conducted with Hymenoptera (ants, bees, and wasps). Here, we show that foundress associations in the haplodiploid social thrips Dunatothrips aneurae (Insecta: Thysanoptera) are most often comprised of close relatives (sisters), though groups with unrelated foundresses are also found. Associations among relatives appear to be facilitated by limited female dispersal, which results in viscous population structure. In addition, we found that per capita productivity declined with increasing group size, sex ratios were female-biased, and some female offspring apparently remained in their natal domicile for some time following eclosion. D. aneurae thus exhibits a suite of similarities with eusocial Hymenoptera, providing evidence for the convergent evolution of associated social and life-history traits in Hymenoptera and Thysanoptera.

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References

  • Aviles L (1997) Causes and consequences of cooperation and permanent-sociality in spiders. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 476–498

    Google Scholar 

  • Bernasconi G, Strassmann JE (1999) Cooperation among unrelated individuals: the ant foundress case. Trends Ecol Evol 14:477–482

    Article  PubMed  Google Scholar 

  • Bono JM, Crespi BJ (2006) Costs and benefits of joint-nesting in Australian Acacia thrips. Insect Soc 53:489–495

    Article  Google Scholar 

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

    Google Scholar 

  • Bouwma AM, Nordheim EV, Jeanne RL (2006) Per-capita productivity in a social wasp: no evidence for a negative effect of colony size. Insect Soc 53:412–419

    Article  Google Scholar 

  • Cahan S, Helms KR, Rissing SW (1998) An abrupt transition in colony founding behaviour in the ant Messor pergandei. Anim Behav 55:1583–1594

    Article  PubMed  Google Scholar 

  • Choe JC, Perman DL (1997) Social conflict and cooperation among founding queens in ants (Hymenoptera: Formicidae). In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Clouse R (2001) Some effects of group size on the output of beginning nests of Mischocyttarus mexicanus (Hymenoptera: Vespidae). Fla Entomol 84:418–425

    Article  Google Scholar 

  • Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72

    Article  PubMed  CAS  Google Scholar 

  • Crespi BJ (2007) Comparative evolutionary ecology of social and sexual systems: water breathing insects come of age. In: Duffy JM, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press

  • Crespi BJ, Choe JC (1997) Explanation and evolution of social systems. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 499–524

    Google Scholar 

  • Crespi BJ, Morris DC, Mound LA (2004) Evolution of ecological and behavioural diversity: Australian Acacia thrips as model organisms. Australian Biological Resources Study and CSIRO, Canberra

    Google Scholar 

  • Danforth BN, Neff JL, Baretto-Ko P (1996) Nestmate relatedness in a communal bee, Perdita texana (Hymenoptera: Andrenidae), based on DNA fingerprinting. Evolution 50:276–284

    Article  CAS  Google Scholar 

  • Fanelli D, Boomsma JJ, Turillazzi S (2005) Multiple reproductive strategies in a tropical hover wasp. Behav Ecol Sociobiol 58:190–199

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2). A computer program to calculate F-statistics. J Heredity 86:485–486

    Google Scholar 

  • Hacker M, Kaib M, Bagine RKN, Epplen JT, Brandl R (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14:1527–1532

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  PubMed  CAS  Google Scholar 

  • Herbers JM (1993) Ecological determinants of queen number in ants. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, New York

    Google Scholar 

  • Ito Y (1993) Behaviour and social evolution of wasps: the communal aggregation hypothesis. Oxford University Press, New York

    Google Scholar 

  • Johnson RA (2004) Colony founding by pleometrosis in the semiclaustral seed-harvester ant Pogonomyrmex californicus (Hymenoptera: Formicidae). Anim Behav 68:1189–1200

    Article  Google Scholar 

  • Karsai I, Wenzel JW (1998) Productivity, individual-level and colony-level flexibility, and organization or work as consequences of colony size. Proc Natl Acad Sci USA 95:8665–8669

    Article  PubMed  CAS  Google Scholar 

  • Kukuk PF, Sage GK (1994) Reproductivity and relatedness in a communal halictine bee Lasioglossum (Chilalictus) hemichalceum. Insect Soc 41:443–455

    Article  Google Scholar 

  • Langer P, Hogendoorn K, Schwarz MP, Keller L (2006) Reproductive skew in the Australian allodapine bee Exoneura robusta. Anim Behav 71:193–201

    Article  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 

  • Liebert AE, Starks PT (2006) Taming of the skew: transactional models fail to predict reproductive partitioning in the paper wasp Polistes dominulus. Anim Behav 71:913–923

    Article  Google Scholar 

  • Maynard Smith J, Szathmary E (1995) The major transitions in evolution. Oxford University Press, New York

    Google Scholar 

  • McCorquodale DB (1988) Relatedness among nestmates in a primitively social wasp, Cerceris antipodes (Hymenoptera: Sphecidae). Behav Ecol Sociobiol 23:401–406

    Article  Google Scholar 

  • Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insect Soc 4:317–344

    Article  Google Scholar 

  • Miller DG (1998a) Consequences of communal gall occupation and a test for kin discrimination in the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae). Behav Ecol Sociobiol 43:95–103

    Article  Google Scholar 

  • Miller DG (1998b) Life history, ecology and communal gall occupation in the manzanita leaf-gall aphid, Tamalia coweni (Cockerell) (Homoptera: Aphididae). J Nat Hist 32:351–366

    Article  Google Scholar 

  • Miller DG (2004) The ecology of inquilinism in communally parasitic Tamalia aphids (Hemiptera: Aphididae). Ann Entomol Soc Am 97:1233–1241

    Article  Google Scholar 

  • Morris DC, Schwarz MP, Crespi BJ (2002) Pleometrosis in phyllode-glueing thrips (Thysanoptera: Phlaeothripidae) on Australian Acacia. Biol J Linn Soc 75:467–474

    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 

  • Paxton RJ, Thoren PA, Tengo J, Estoup A, Pamilo P (1996) Mating structure and nestmated relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519

    Article  PubMed  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

  • Queller DC, Zacchi F, Cervo R, Turillazzi S, Henshaw MT, Santorelli LA, Strassmann JE (2000) Unrelated helpers in a social insect. Nature 405:784–787

    Article  PubMed  CAS  Google Scholar 

  • Reeve HK (1991) Polistes. In: Ross KG, Mathews RW (eds) The social biology of wasps. Comstock Publishing Associates, Ithaca

    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 

  • Saito Y (1997) Sociality and kin selection in Acari. In: Crespi BJ, Choe JC (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 443–457

    Google Scholar 

  • Schwarz MP, Bull NJ, Hogendoorn K (1998) Evolution of sociality in the allodapine bees: a review of sex allocation, ecology and evolution. Insect Soc 45:349–368

    Article  Google Scholar 

  • Schwarz MP, O’keefe KJ (1991) Cooperative nesting and ovarian development in females of the predominantly social bee Exoneura bicolor Smith after forced solitary eclosion. J Aust Entomol Soc 30:251–255

    Article  Google Scholar 

  • Schwarz MP, Silberbauer LX, Hurst PS (1997) Intrinsic and extrinsic factors associated with social evolution in allodapine bees. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Shellman-Reeve JS (1997) The spectrum of eusociality in termites. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Silberbauer LX, Schwarz MP (1995) Life cycle and social behaviour in a heathland population of the allodapine bee, Exoneura bicolor (Hymenoptera: Apidae). Insect Soc 42:201–218

    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 

  • Soucy SL, Giray T, Roubik DW (2003) Solitary and group nesting in the orchid bee Euglossa hyacinthina (Hymenoptera, Apidae). Insect Soc 50:248–255

    Article  Google Scholar 

  • Strassmann JE, Queller DC (1989) Ecological determinants of social evolution. In: Breed M, Page R (eds) The genetics of social evolution. Westview, Boulder

    Google Scholar 

  • Uetz GW, Hieber CS (1997) Colonial web-building spiders: balancing the costs and benefits of group living. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

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Acknowledgements

We would like to thank Mike Schwarz and Tom Chapman for providing lab space and organizing field logistics as well as Laurence Mound and David Morris for the help in collecting samples. We also thank David Queller for his assistance with the maximum likelihood analysis and three anonymous reviewers for the constructive comments on the manuscript. This research was funded by an NSF International Research Fellowship to J.M.B and an NSERC grant to B.J.C.

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Correspondence to Jeremy M. Bono.

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Communicated by L. Keller

Appendices

Appendix 1

Table 3 Summary of D. aneurae colony samples from two collecting trips to New South Wales (NSW) and South Australia (SA)

Appendix 2

Table 4 Primer sequences, number of alleles, H o (observed heterozygosity), and allele size ranges for three microsatellites used to analyze cofoundress relatedness

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Bono, J.M., Crespi, B.J. Cofoundress relatedness and group productivity in colonies of social Dunatothrips (Insecta: Thysanoptera) on Australian Acacia . Behav Ecol Sociobiol 62, 1489–1498 (2008). https://doi.org/10.1007/s00265-008-0578-4

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