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Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species

Published online by Cambridge University Press:  01 July 2008

L. Leniaud
Affiliation:
IRBI CNRS UMR 6035 Université François Rabelais, Faculté des Sciences et Techniques, Parc de Grandmont, 37200 Tours, France
A. Pichon
Affiliation:
IRBI CNRS UMR 6035 Université François Rabelais, Faculté des Sciences et Techniques, Parc de Grandmont, 37200 Tours, France
P. Uva
Affiliation:
Istituto di Ricerche di Biologia Molecolare, Merck Research Laboratories, 00040 Pomezia, Rome, Italy
A.-G. Bagnères*
Affiliation:
IRBI CNRS UMR 6035 Université François Rabelais, Faculté des Sciences et Techniques, Parc de Grandmont, 37200 Tours, France
*
*Author for correspondence Fax: +33 247367356 E-mail: [email protected]

Abstract

Social insects are among the world's most successful species at invading of new habitats. A good example of this invasive ability is Reticulitermes (Rhinotermitidae), a prominent group of subterranean termites. As a result of human intervention, i.e. transportation and creation of urban heat islands, Reticulitermes have been able to invade and thrive in cities located in areas where the natural habitat is normally too cold for colonization. They commonly infest man-made structures where they can cause extensive damage.

This study was designed to evaluate the invasiveness of Reticulitermes urbis that was probably introduced in France from the Balkans. Invasive potential was assessed on the basis of features typical to invasive social insects, i.e. unicoloniality, low intraspecific aggression, high level of polygyny and colony reproduction by budding. The opportunity to study establishment and spreading processes arose after extensive sampling of an imported Reticulitermes urbis population was performed over the entire city of Domène, France (Rhône-Alpes region).

For the first time, genetic analysis showed that the termites belonged to a single ‘genetic entity’ forming a vast colony covering about seven hectares. The colony was structured as an extended family with separate reproductive centres. We speculate that termites were introduced in a single location from which they gradually budded throughout the old town. Based on the absence of aggression among different nests within the colony, we defined this ‘genetic entity’ as a supercolony.

Type
Research Paper
Copyright
Copyright © 2008 Cambridge University Press

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References

Abbott, K.L. (2006) Spatial dynamics of supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on Christmas Island, Indian Ocean. Diversity and Distributions 12, 101110.CrossRefGoogle Scholar
Atkinson, L. & Adams, E.S. (1997) The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proceedings of the Royal Society of London, Series B 264, 11311136.CrossRefGoogle Scholar
Austin, J.W., Szalanski, A.L., Scheffrahn, R.H., Messenger, M.T., Dronnet, S. & Bagnères, A.G. (2005) Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Annals of the Entomological Society of America 98(3), 395401.CrossRefGoogle Scholar
Bagnères, A.-G. (1989) Les hydrocarbures cuticulaires des insectes sociaux: Détermination et rôle dans la reconnaissance spécifique, coloniale et individuelle. PhD thesis, Université Pierre et Marie Curie, Paris VI.Google Scholar
Bagnères, A.-G., Clément, J.-C., Blum, M.S., Severson, R.F., Joulie, C. & Lange, C. (1990) Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): polymorphism and chemotaxonomy. Journal of Chemical Ecology 16(12), 32133244.CrossRefGoogle Scholar
Bagnères, A.-G., Uva, P. & Clément, J.-L. (2003) Description d'une nouvelle espèce de Termite: Reticulitermes urbis n.sp. (Isopt., Rhinotermitidae). Bulletin de la Société Entomologique de France 108(4), 433435.Google Scholar
Begon, M. (1979) Investigating Animal Abundance: Capture-recapture for Biologists. 97 pp. Baltimore, MD, USA, University Park Press.Google Scholar
Bulmer, M.S. & Traniello, J.F.A. (2002) Foraging range expansion and colony genetic organization in the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae). Environmental Entomology 31(2), 293298.CrossRefGoogle Scholar
Bulmer, M.S., Adams, E.S. & Traniello, J.F.A. (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behavioral Ecology and Sociobiology 49, 236243.CrossRefGoogle Scholar
Chapman, R.E. & Bourke, A.F.G. (2001) The influence of sociality on the conservation biology of social insects. Ecology Letters 4, 650662.CrossRefGoogle Scholar
Clément, J.-L. (1978) L'agression interspécifique et intraspécifique des espèces françaises du genre Reticulitermes (Isoptère). Comptes Rendus de l'Académie des Sciences de Paris 286(D), 351354.Google Scholar
Clément, J.-L. (1981) Enzymatic polymorphism in the European populations of various Reticulitermes species (Isoptera). pp. 4962in Howse, P.E. & Clément, J.-L. (Eds) Biosystematics of Social Insects, vol. 19. London, Academic Press.Google Scholar
Clément, J-L. (1986) Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae): geographic and seasonal variations. Sociobiology 11, 311323.Google Scholar
Clément, J.-L., Bagnères, A.-G., Uva, P., Wilfert, L., Quintana, A., Reinhard, J. & Dronnet, S. (2001) Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insectes sociaux 48, 202215.CrossRefGoogle Scholar
Corin, S.E., Abbott, K.L., Ritchie, P.A. & Lester, P.J. (2007) Large scale unicoloniality: the population and colony structure of the invasive Argentine ant (Linepithema humile) in New Zealand. Insectes Sociaux 54(3), 275282.CrossRefGoogle Scholar
DeHeer, C.J. & Vargo, E.L. (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Molecular Ecology 13, 431441.CrossRefGoogle ScholarPubMed
Dronnet, S., Bagnères, A.G., Juba, T.R. & Vargo, E.L. (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Molecular Ecology Notes 4(1), 127129.CrossRefGoogle Scholar
Dronnet, S., Chapuisat, M., Vargo, E.L., Lohou, C. & Bagnères, A.G. (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Molecular Ecology 14(5), 13111320.CrossRefGoogle Scholar
Easey, J.F. & Holt, J.A. (1989) Population estimation of some mound-building termites (Isoptera, termitidae) using radioisotope methods. Material und Organismen 24(2), 8191.Google Scholar
Evans, T.A., Lenz, M. & Gleeson, P.V. (1998) Testing assumptions of mark-recapture protocols for estimating population size using Australian mound-building, subterranean termites. Ecological Entomology 23, 139159.CrossRefGoogle Scholar
Evans, T.A., Lenz, M. & Gleeson, P.V. (1999) Estimating population size and forager movement in a tropical subterranean termite (Isoptera: Rhinotermitidae). Environmental Entomology 28(5), 823830.CrossRefGoogle Scholar
Ferrari, R., Marini, M., Tiglié, I. & Zaffagnini, V. (1998) Indagine sulle popolazioni di termiti Reticulitermes lucifugus Rossi (Isopptera: Rhinotermitidae) con metodiche di tripla marcatura e ricattura. Disinfestazione & igiene ambientale 15(1), 1420.Google Scholar
Forschler, B.T. & Jenkins, T.M. (1999) Evaluation of subterranean termite biology using genetic, chemotaxonomic, and morphometric markers and ecological data: a testimonial for multidisciplinary efforts. Trends in Entomology 2, 7280.Google Scholar
Gay, F.J. (1969) Species introduced by man. pp. 459494in Krishna, K. & Weesner, F.M. (Eds) Biology of Termites, vol. 1. New York, Academic Press.CrossRefGoogle Scholar
Giraud, T., Pedersen, J.S. & Keller, L. (2002) Evolution of supercolonies: The Argentine ants of southern Europe. Proceedings of the National Academy of Science of the United States of America 99, 60756079.CrossRefGoogle ScholarPubMed
Goodisman, M.A.D. & Crozier, R.H. (2002) Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56, 7083.Google ScholarPubMed
Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignement editor and analysis program for Windows 95/98/NT. Nuclear Acids Symposium Series 41, 9598.Google Scholar
Haverty, M.I., Nelson, L.J. & Page, R.E. (1991) Preliminary investigations of the cuticular hydrocarbons from North American Reticulitermes and tropical and subtropical Coptotermes (Isoptera: Rhinotermitidae) for chemotaxonomic studies. Sociobiology 19, 5176.Google Scholar
Holtzer, B., Chapuisat, M., Kremer, N., Finet, C. & Keller, L. (2006) Unicoloniality, recognition and genetic differentiation in a native Formica ant. Journal of Evolutionary Biology 19(6), 20312039.CrossRefGoogle Scholar
Holway, D.A., Suarez, A.V. & Case, T.J. (1998) Loss of Intraspecific Aggression in the Success of a Widespread Invasive Social Insect. Science 282, 949952.CrossRefGoogle ScholarPubMed
Holway, D.A., Lach, L., Suarez, A.V., Tsutsui, N.D. & Case, T.J. (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics 33, 181233.CrossRefGoogle Scholar
Husseneder, C. & Grace, J.K. (2001) Similarity is relative: hierarchy of genetic similarities in the Formosan subterranean termite (Isoptera: Rhinotermitidae) in Hawaii. Environmental Entomology 30, 262266.CrossRefGoogle Scholar
Husseneder, C., Messenger, M.T., Su, N.Y., Grace, J.K. & Vargo, E.L. (2005) Colony social organization and population genetic structure of an introduced population of Formosan subterranean termite from New Orleans, Louisiana. Journal of Economic Entomology 98(5), 14211434.CrossRefGoogle ScholarPubMed
Lainé, L.V. (2002) Biological studies on two European termite species: establishment risk in the UK. PhD thesis, Imperial College, Ascot, UK.Google Scholar
Lainé, L.V. & Wright, D.J. (2003) The life cycle of Reticulitermes spp. (Isoptera: Rhinotermitidae): what do we know? Bulletin of Entomological Research 93, 267278.CrossRefGoogle ScholarPubMed
Lebreton, J.D., Pradel, R. & Clobert, J. (1993) The Statistical-Analysis of Survival in Animal Populations. Trends in Ecology & Evolution 8(3), 9195.CrossRefGoogle ScholarPubMed
Lindberg, M. & Rexstad, E. (2002) Capture-recapture sampling designs. pp. 251262in El-Shaarawi, A.H. & Piegorsh, W.W. (Eds) Encyclopedia of Environmetrics. Chichester, UK, Wiley & Sons.Google Scholar
Luchetti, A., Trenta, M., Mantovani, B. & Marini, M. (2004) Taxonomy and phylogeny of north mediterranean Reticulitermes (Isoptera, Rhinotermitidae): a new insight. Insectes Sociaux 51, 117122.CrossRefGoogle Scholar
Luchetti, A., Marini, M. & Mantovani, B. (2007) Filling the gap: biosystematics of the eusocial system Reticulitermes (Isoptera, Rhinotermitidae) in the Balkanic Pennsula and Aegean area. Molecular Phylogenetics and Evolution 45(1), 377383.CrossRefGoogle Scholar
Marini, M. & Mantovani, B. (2002) Molecular Relationships among European Samples of Reticulitermes (Isoptera, Rhinotermitidae). Molecular Phylogenetics and Evolution 22(3), 454459.CrossRefGoogle ScholarPubMed
Miura, T., Roisin, Y. & Matsumoto, T. (2000) Phylogeny and biogeography of the nasute termite genus Nasutitermes (Isoptera: Termitidae) in the Pacific Tropics. Molecular Phylogenetics and Evolution 22, 454459.Google Scholar
Moller, H. (1996) Lessons for invasion theory from social insects. Biological Conservation 78, 125142.CrossRefGoogle Scholar
Paulmier, I., Vauchot, B., Pruvost, A.-M., Lohou, C., Tussac, M., Jéquel, M., Leca, J.-L. & Clément, J.-L. (1997) Evaluation of two populations of Reticulitermes santonensis De Feytaud (Isoptera) by triple mark-recapture procedure. pp. 25 in Proceedings, 28th Annual Meeting of the International Research Group on Wood Preservation. International Research Group on Wood Preservation, 26–30 May 1997, Whistler, BC, Canada.Google Scholar
Pichon, A., Kutnik, M., Leniaud, L., Darrouzet, E., Châline, N., Dupont, S. & Bagnères, A.-G. (2007) Development of experimentally orphaned termite worker colonies of two Reticulitermes species. Sociobiology 50(3), 10151034.Google Scholar
Raymond, M. & Rousset, F. (1995) An exact test for population differentiation. Evolution 49(6), 12801283.CrossRefGoogle ScholarPubMed
Ross, K.G. (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Molecular Ecology 10, 265284.CrossRefGoogle ScholarPubMed
Rousset, F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 12191228.CrossRefGoogle ScholarPubMed
Schneider, S.S., DeGrandi-Hoffman, G., Scott, S. & Roan Smith, D. (2003) The African honey bee: factors contributing to a successful biological invasion. Annual Review of Entomology 49, 351376.CrossRefGoogle Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Annals of the Entomological Society of America 87(6), 651701.CrossRefGoogle Scholar
Slatkin, M. (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47, 264279.CrossRefGoogle ScholarPubMed
Su, N.Y. & Scheffrahn, R.H. (1993) Laboratory evaluation of two chitin synthesis inhibitors, hexaflumuron and diflubenzuron, as bait toxicants against formosan and eastern subterranean termites (Isoptera, Rhinotermitidae). Journal of Economic Entomology 86(5), 14531457.CrossRefGoogle Scholar
Su, N.Y. & Scheffrahn, R.H. (2000) Termites as pests of buildings. pp. 437453in Abe, T., Bignell, D. & Higashi, M. (Eds) Termites, Evolution, Sociality, Symbioses, Ecology. Dordrecht, The Netherlands, Kluwer Academic Publisher.CrossRefGoogle Scholar
Su, N.Y., Ban, P.M. & Scheffrahn, R.H. (1993) Foraging populations and territories of the eastern subterranean termite (Isoptera, Rhinotermitidae) in southeastern Florida. Environmental Entomology 22(5), 11131117.CrossRefGoogle Scholar
Sundstrom, L. & Boomsma, J.J. (2001) Conflicts and alliances in insect families. Heredity 86, 515521.CrossRefGoogle ScholarPubMed
Swetnam, T.W. & Lynch, A.M. (1993) Multicentury, regional-scale patterns of western spruce budworm outbreaks. Ecological Monographs 63, 399424.CrossRefGoogle Scholar
Thomas, M.L., Payne-Makrisa, C.M., Suarez, A.V., Tsutsui, N.D. & Holway, D.A. (2006) When supercolonies collide: territorial aggression in an invasive and unicolonial social insect. Molecular Ecology 15, 43034315.CrossRefGoogle Scholar
Thompson, G.J. & Hebert, P.D.N. (1998) Population genetic structure of the Neotropical termite Nasutitermes costalis (Isoptera: Termitidae). Heredity 80, 4855.CrossRefGoogle Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) Clustal-w – Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22(22), 46734680.CrossRefGoogle ScholarPubMed
Thorne, B.L., Traniello, J.F.A., Adams, E.S. & 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. Ethology Ecology and Evolution 11, 149169.CrossRefGoogle Scholar
Tsutsui, N.D. & Suarez, A.V. (2003) The colony structure and population biology of invasive ants. Conservation Biology 17(1), 4858.CrossRefGoogle Scholar
Tsutsui, N.D., Suarez, A.V., Holway, D.A. & Case, T.J. (2000) Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America 97, 59485953.CrossRefGoogle ScholarPubMed
Uva, P. (2002) Relations phylogénétiques chez les termites du genre Reticulitermes en Europe. Description d'une nouvelle espèce. PhD thesis, Université François Rabelais, Tours.Google Scholar
Uva, P., Clément, J.-L., Austin, J.W., Aubert, J., Zaffagnini, V., Quintana, A. & Bagnères, A.-G. (2004) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Molecular Phylogenetics and Evolution 30, 344353.CrossRefGoogle ScholarPubMed
Vargo, E.L. (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Molecular Ecology 9, 817829.CrossRefGoogle ScholarPubMed
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. Environmental Entomology 32(5), 12711282.CrossRefGoogle Scholar
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(12), 28052818.Google ScholarPubMed
Vargo, E.L., Husseneder, C., Grace, J.K., Henderson, G. & Ring, D. (2003) Colony and population genetic structure of subterranean termites from Hawaii and Louisiana. Sociobiology 41(1A), 6769.Google Scholar
Walsh, P.S., Metzger, D.A. & Higuchi, R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10(4), 506513.Google ScholarPubMed
Williams, D.F. (Ed.) (1994) Exotic Ants. Biology, Impact and Control of Social Introduced Species. 332 pp. Boulder, CO, USA, Westview Press.Google Scholar
Williams, D.W. & Liebhold, A.M. (1995) Forest defoliators and climatic change: potential changes in spatial distribution of outbreaks of western spruce budworm (Lepidoptera: Tortricidae) and gypsy moth (Lepidoptera: Lymantriidae). Environmental Entomology 24, 19.CrossRefGoogle Scholar
Zayed, A., Constantin, Ş.A. & Packer, L. (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2(9).CrossRefGoogle ScholarPubMed