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High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes

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Abstract

The coexistence of multiple unrelated reproductives within social insect colonies decreases the relatedness among colony members and therefore challenges kin selection theory. This study investigated the colony genetic structure of a French introduced population of the American subterranean termite Reticulitermes flavipes by analyzing genotypes at eight microsatellite loci and at one mtDNA region. Results revealed that all colonies contained numerous related secondary reproductives, and that 31% of colonies possessed more than two unrelated reproductives. The presence of several unrelated reproductives within colonies of this species is commonly assumed to result from colony fusion. Although such a high occurrence of colony fusion is the highest ever observed in a termite population, it is probable that the available methodology underestimated the detection of colony fusion in French populations. Overall, these results suggest that French colonies might differ strongly from the great majority of American colonies in their capacity to produce secondary reproductives as well as in their ability to merge. The nature and evolutionary origin of these population differences are discussed.

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References

  • Adams E.S., Atkinson L. and Bulmer M.S. 2007. Relatedness, recognition errors, and colony fusion in the termite Nasutitermes corniger. Behav. Ecol. Sociobiol. 61: 1195-1201

    Google Scholar 

  • Atkinson L. and Adams E.S. 1997. The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proc. R. Soc. Lond. B Biol. Sci. 264: 1131-1136

    Google Scholar 

  • Austin J.W., Szalanski A.L., Scheffrahn R.H., Messenger M.T., Dronnet S. and Bagnères A.G. 2005. Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Ann. Entomol. Soc. Am. 98: 395-401

  • Bourke A.F.G. and Franks N.R. (Eds) (1995) Social Evolution in Ants, Princeton Univ. Press, Princeton. 550 pp

  • Bulmer M.S., Adams E.S. and Traniello J.F.A. 2001. Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav. Ecol. Sociobiol. 49: 236-243

    Google Scholar 

  • Bulmer M.S. and Traniello J.F.A. 2002a. Foraging range expansion and colony genetic organization in the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae). Environ. Entomol. 31: 293-298

  • Bulmer M.S. and Traniello J.F.A. 2002b. Lack of aggression and spatial association of colony members in Reticulitermes flavipes. J. Insect Behav. 15: 121-126

  • Buttermore R.E. 1997. Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in southern Tasmania. Aust. J. Entomol. 36: 251-254

    Google Scholar 

  • Chapman R.E. and Bourke A.F.G. 2001. The influence of sociality on the conservation biology of social insects. Ecol. Lett. 4: 650-662

    Google Scholar 

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

    Google Scholar 

  • Clément J.-L., Bagnères A.-G., Uva P., Wilfert L., Quintana A., Reinhard J. and Dronnet S. 2001. Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insect. Soc. 48: 202-215

    Google Scholar 

  • DeHeer C.J. and Kamble S.T. 2008. Colony genetic organization, fusion and inbreeding in Reticulitermes flavipes from the Midwestern U.S. Sociobiology 51: 307-325

  • DeHeer C.J. and Vargo E.L. 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

    Google Scholar 

  • DeHeer C.J. and Vargo E.L. 2006. An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav. Ecol. Sociobiol. 59: 753-761

    Google Scholar 

  • DeHeer C.J. and Vargo E.L. 2008. Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the termite Reticulitermes flavipes. Insect. Soc. 55: 190-199

    Google Scholar 

  • Donovan B.J., Howie A.M.E., Schroeder N.C., Wallace A.R. and Read P.E.C. 1992. Comparative characteristics of nests of Vespula germanica (F) and Vespula vulgaris (L) (Hymenoptera, Vespinae) from Christchurch-city, New-Zealand. N.Z. J. Zool. 19: 61-71

  • Dronnet S., Bagnères A.-G., Juba T.R. and Vargo E.L. 2004. Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol. Ecol. Notes 4: 127-129

  • Dronnet S., Chapuisat M., Vargo E.L., Lohou C. and Bagnères A.G. 2005. Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol. Ecol. 14: 1311-1320

    Google Scholar 

  • Fournier D., de Biseau J.C. and Aron S. 2009. Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala. Mol. Ecol. 18: 186-199

    Google Scholar 

  • Giraud T., Pedersen J.S. and Keller L. 2002. Evolution of supercolonies: The Argentine ants of southern Europe. Proc. Natl Acad. Sci. USA 99: 6075-6079

    Google Scholar 

  • Goodisman M.A.D. and Crozier R.H. 2002. Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56: 70-83

    Google Scholar 

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

    Google Scholar 

  • Grace J.K., Abdallay A. and Farr K.R. 1989. Eastern subterranean termite (isoptera: Rhinotermitidae) foraging territories and populations in Toronto. Can. Entomol. 121: 551-556

    Google Scholar 

  • Hacker M., Kaib M., Bagine R.K.N., Epplen J.T. and Brandl R. 2005. Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol. Ecol. 14: 1527-1532

    Google Scholar 

  • Hall T.A. 1999. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclear Acids Symposium Series 41: 95-98

  • Heinze J. and Foitzik S. (2009) The Evolution of queen numbers in ants: from one to many and back. In: Organization of Insect Societies, from Genome to Sociocomplexity (Gadau J. and Fewell J., Eds). University of Harvard Press, pp 26-50.

  • Helanterä H., Strassmann J.E., Carrillo J. and Queller D.C. 2009. Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol. Evol. 24: 341-349.

    Google Scholar 

  • Hölldobler B. and Wilson E.O. 1990. The Ants. The Belknap Press of Harvard University Press, Cambridge, Massachusetts. 732 pp

  • Holway D.A., Lach L., Suarez A.V., Tsutsui N.D. and Case T.J. 2002. The causes and consequences of ant invasions. Annu. Rev. Ecol. Syst. 33: 181-233

    Google Scholar 

  • Holzer B., Chapuisat M., Kremer N., Finet C. and Keller L. 2006. Unicoloniality, recognition and genetic differentiation in a native Formica ant. J. Evol. Biol. 19: 2031-2039

    Google Scholar 

  • Jenkins T.M., Dean R.E., Verkerk R. and Forschler B.T. 2001. Phylogenetic analyses of two mitochondrial genes and one nuclear intron region illuminate European subterranean termite (Isoptera: Rhinotermitidae) gene flow, taxonomy, and introduction dynamics. Mol. Phylogenet. Evol. 20: 286-293

    Google Scholar 

  • Johns P.M., Howard K.J., Breisch N.L., Rivera A. and Thorne B.L. 2009. Nonrelatives inherit colony resources in a primitive termite. Proc. Natl Acad. Sci. USA 106: 17452-17456

    Google Scholar 

  • Kasper M.L., Reeson A.F. and Austin A.D. 2008. Colony characteristics of Vespula germanica (F.) (Hymenoptera, Vespidae) in a Mediterranean climate (southern Australia). Aust. J. Entomol. 47: 265-274

    Google Scholar 

  • Keller L. 1993. The assessment of reproductive success of queens in ants and other social insects. Oikos 67: 177-180

    Google Scholar 

  • Korb J. 2008. Termites, hemimetabolous diploid white ants? Front. Zool. 5: 15

    Google Scholar 

  • Le Breton J., Delabie J.H.C., Chazeau J., Dejean A. and Jourdan H. 2004. Experimental evidence of large-scale unicoloniality in the tramp ant Wasmannia auropunctata (Roger). J. Insect Behav. 17: 263-271

    Google Scholar 

  • Legendre F., Whiting M.F., Bordereau C., Cancello E.M., Evans T.A. and Grandcolas P. 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

    Google Scholar 

  • Leniaud L. 2008. Potentialités ontogéniques, différenciation des castes et conséquences sur la structure génétique des termites du genre Reticulitermes. University of Tours (François Rabelais), Tours, pp 193

  • Leniaud L., Pichon A., Uva P. and Bagnères A.G. 2009. Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species Bull. Entomol. Res. 99: pp 1-10

    Google Scholar 

  • Leniaud L., Dedeine F., Pichon A., Dupont S. and Bagnères A.-G. 2010. Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae) Biol. Invasions 12: 1389-1402

    Google Scholar 

  • Lenz M. and Barrett R.A. 1982. Neotenic formation in field colonies of Coptotermes lacteus (Froggatt) in Australia, with comments on the roles of neotenics in the genus Coptotermes (Isoptera: Rhinotermitidae). Sociobiology 7: 47-59

  • Matsuura K. 2001. Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92: 20-26

    Google Scholar 

  • Miura T., Roisin Y. and Matsumoto T. 2000. Molecular phylogeny and biogeography of the nasute termite genus Nasutitermes (Isoptera : Termitidae) in the Pacific tropics. Mol. Phylogenet. Evol. 17: 1-10

    Google Scholar 

  • Morel L., Vander Meer R.K. and Lofgren C.S. 1990. Comparison of nestmate recognition between monogyne and polygyne populations of Solenopsis invicta (Hymenoptera, Formicidae). Ann. Entomol. Soc. Am. 83: 642-647

    Google Scholar 

  • Myles T.G. 1999. Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33: 1-43

    Google Scholar 

  • Nagamitsu T. and Yamagishi H. 2009. Nest density, genetic structure, and triploid workers in exotic Bombus terrestris populations colonized Japan. Apidologie 40: 429-440

    Google Scholar 

  • Nei M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New-York. 512 pp

  • Nobre T., Nunes L. and Bignell D.E. 2008. Colony interactions in Reticulitermes grassei population assessed by molecular genetic methods. Insect. Soc. 55: 66-73

    Google Scholar 

  • Orivel J., Grangier J., Foucaud J., Le Breton J., Andrès F.X., Jourdan H., Delabie J.H.C., Fournier D., Cerdan P., Facon B., Estoup A. and Dejean A. 2009. Ecologically heterogeneous populations of the invasive ant Wasmannia auropunctata within its native and introduced ranges. Ecol. Entomol. 34: 504-512

    Google Scholar 

  • Parman V. and Vargo E.L. 2008. Population density, species abundance, and breeding structure of subterranean termite colonies in and around infested houses in central North Carolina. J. Econ. Entomol. 101: 1349-1359

    Google Scholar 

  • Pedersen J.S., Krieger M.J.B., Vogel V., Giraud T. and Keller L. 2006. Native supercolonies of unrelated individuals in the invasive Argentine ant. Evolution 60: 782-791

    Google Scholar 

  • Pichon A., Kutnik M., Leniaud L., Darrouzet E., Chaline N., Dupont S. and Bagnères A.G. 2007. Development of experimentally orphaned termite worker colonies of two Reticulitermes species (Isoptera : Rhinotermitidae). Sociobiology 50: 1015-1034

    Google Scholar 

  • Queller D.C. and Goodnight K.F. 1989. Estimating relatedness using genetic markers. Evolution 43: 258-275

    Google Scholar 

  • Raymond M. and Rousset F. 1995. An exact test for population differentiation. Evolution 49: 1280-1283

    Google Scholar 

  • Sambrook J., Fritcsh E.F. and Maniatis T. 1989. Molecular Cloning. 2nd Ed. Cold Spring Harbor Lab Press, Cold Spring Harbor, NY. 253 pp

  • Shelton T.G. and Grace J.K. 1996. Review of agonistic behaviors in the Isoptera. Sociobiology 28: 155-176

    Google Scholar 

  • Simon C., Frati F., Beckenbach A., Crespi B., Liu H. and Flook P. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann. Entomol. Soc. Am. 87: 651-701

    Google Scholar 

  • Su N.Y., Ye W.M., Ripa R., Scheffrahn R.H. and Giblin-Davis R.M. 2006. Identification of Chilean Reticulitermes (Isoptera:Rhinotermitidae) inferred from three mitochondrial gene DNA sequences and soldier morphology. Ann. Entomol. Soc. Am. 99: 352-363

    Google Scholar 

  • Thompson J.D., Higgins D.G. and Gibson T.J. 1994b. Clustal-w - Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific, gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680

  • Thorne B.L., Traniello J.F.A., Adams E.S. and Bulmer M. 1999. Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological and genetic studies. Ethol. Ecol. Evol. 11: 149-169

    Google Scholar 

  • Tsutsui N.D. and Suarez A.V. 2003. The colony structure and population biology of invasive ants. Conserv. Biol. 17: 48-58

    Google Scholar 

  • Tsutsui N.D., Suarez A.V., Holway D.A. and Case T.J. 2000. Reduced genetic variation in the success of an invasive species. Proc. Natl Acad. Sci. USA 97: 5948-5953.

    Google Scholar 

  • Vanloon A.J., Boomsma J.J. and Andrasfalvy A. 1990. A new polygynous Lasius species (Hymenoptera, Formicidae) from Central-Europe. 1. Description and general biology. Insect. Soc. 37: 348-362

    Google Scholar 

  • Vargo E.L. 2000. Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol. Ecol. 9: 817-829

    Google Scholar 

  • Vargo E.L. 2003a. Genetic structure of Reticulitermes flavipes and R. virginicus (Isoptera : Rhinotermitidae) colonies in an urban habitat and tracking of colonies following treatment with hexaflumuron bait. Environ. Entomol. 32: 1271-1282

  • Vargo E.L. 2003b. Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57: 2805-2818

  • Vargo E.L. and Carlson J.R. 2006. Comparative study of breeding systems of sympatric subterranean termites (Reticulitermes flavipes and R. hageni) in Central North Carolina using two classes of molecular genetic markers. Environ. Entomol. 35: 173-187

    Google Scholar 

  • Vargo E.L. and Husseneder C. 2009. Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu. Rev. Entomol. 54: 379-403

    Google Scholar 

  • Vargo E.L., Juba T.R. and DeHeer C.J. 2006. Relative abundance and comparative breeding structure of subterranean termite colonies (Reticulitermes flavipes, Reticulitermes hageni, Reticulitermes virginicus, and Coptotermes formosanus) in a South Carolina lowcountry site as revealed by molecular markers. Ann. Entomol. Soc. Am. 99: 1101-1109

    Google Scholar 

  • Vogel V., Pedersen J.S., d’Ettorre P., Lehmann L. and Keller L. 2009. Dynamics and genetic structure of Argentine ant supercolonies in their native range. Evolution 63: 1627-1639

    Google Scholar 

  • Weir B.S. and Cockerham C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370

    Google Scholar 

  • Wilson E.O. and Hölldobler B. 2005. Eusociality: Origin and consequences. Proc. Natl Acad. Sci. USA 102: 16119-16119

    Google Scholar 

  • Ye W., Lee C.-Y., Scheffrahn R.H., Aleong J.M., Su N.-Y., Bennett G.W. and Scharf M.E. 2004. Phylogenetic relationships of nearctic Reticulitermes species (Isoptera: Rhinotermitidae) with particular reference to Reticulitermes arenincola Goellner. Mol. Phylogenet. Evol. 30: 815-822

    Google Scholar 

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Acknowledgments

We wish to thank Ed Vargo and Stéphanie Dronnet-Bankhead for their helpful comments on the manuscript, as well as Charles Edouart Imbert for its technical assistance. We also wish to thank Tony Tebby for his help to improve the English of the manuscript.

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Perdereau, E., Bagnères, AG., Dupont, S. et al. High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes . Insect. Soc. 57, 393–402 (2010). https://doi.org/10.1007/s00040-010-0096-z

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