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Mitochondrial and nuclear markers highlight the biodiversity of Kalotermes flavicollis (Fabricius, 1793) (Insecta, Isoptera, Kalotermitidae) in the Mediterranean area

Published online by Cambridge University Press:  13 January 2011

A. Velonà
Affiliation:
Università degli Studi di Bologna, Dipartimento di Biologia Evoluzionistica Sperimentale, via Selmi 3, 40126 Bologna, Italy
A. Luchetti
Affiliation:
Università degli Studi di Bologna, Dipartimento di Biologia Evoluzionistica Sperimentale, via Selmi 3, 40126 Bologna, Italy
S. Ghesini
Affiliation:
Università degli Studi di Bologna, Dipartimento di Biologia Evoluzionistica Sperimentale, via Selmi 3, 40126 Bologna, Italy
M. Marini
Affiliation:
Università degli Studi di Bologna, Dipartimento di Biologia Evoluzionistica Sperimentale, via Selmi 3, 40126 Bologna, Italy
B. Mantovani*
Affiliation:
Università degli Studi di Bologna, Dipartimento di Biologia Evoluzionistica Sperimentale, via Selmi 3, 40126 Bologna, Italy
*
*Author for correspondence Fax: 0039 0512094286 E-mail: barbara.mantovani@unibo.it

Abstract

The biodiversity of the European termite Kalotermes flavicollis is here studied through the analysis of mitochondrial (303 bp of control region and 912 bp of COI/tRNALeu/COII) and nuclear (five microsatellite and 20 Inter-SINE loci) markers on 18 colonies collected in Southern France, Corsica, Sardinia, peninsular Italy, the Balkans and Greece. Different statistical analyses (Bayesian phylogenetic analysis, parsimony network, F-statistics, PCA) were performed. Mitochondrial sequences produced an unresolved polytomy including samples from peninsular Italy, Balkans and Greece, and three main clades: southern France, Corsica-Sardinia and Portoscuso (SW Sardinia). Nuclear markers confirm these data, further highlighting a more significant divergence at the regional scale. The results obtained for the peri-Tyrrhenian area agree with major paleogeographic and paleoclimatic events that shaped the biodiversity of the local fauna. K. flavicollis biodiversity and its phylogeographic pattern are also evaluated in the light of the data available for the other native European termite taxon (genus Reticulitermes), in order to produce a more complete scenario of the Mediterranean. In the area comprised between southern France and Italy, the degree of diversity is similar; however, in the eastern area, while K. flavicollis is differentiated only at the population level, the genus Reticulitermes comprises at least six entities of specific and/or subspecific level. This discrepancy may be explained by taking into account the different evolutionary histories of the two taxa.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Arbogast, B.S. & Kenagy, G.J. (2001) Comparative phylogeography as an integrative approach to historical biogeography. Journal of Biogeography 28, 819825.CrossRefGoogle Scholar
Austin, J.W., Szalanski, A.L., Uva, P., Bagnères, A.G. & Kence, A. (2002) A comparative genetic analysis of the subterranean termite genus Reticulitermes (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America 95, 753760.CrossRefGoogle Scholar
Belkhir, K., Borsa, P., Chikki, L., Raufaste, N. & Bonhomme, F. (2003) GENETIX, logiciel sous Windows TM pour la génétique des populations. Available online at http://www.genetix.univ-montp2.fr/genetix/genetix.htm.Google Scholar
Benson, G. (1999) Tandem Repeat Finder: a program to analyze DNA sequences. Nucleic Acids Research 27, 573580.CrossRefGoogle Scholar
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571660.CrossRefGoogle ScholarPubMed
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
Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochemical Bulletin 19, 1115.Google Scholar
Eggleton, P. & Tayasu, I. (2001) Feeding groups, lifetype and the global ecology of termites. Ecological Research 16, 941960.CrossRefGoogle Scholar
Engel, M.S. & Krishna, K. (2004) Family-group names for termites (Isoptera). American Museum Novitates 2570, 131.Google Scholar
Engel, M.S., Grimaldi, D.A. & Krishna, K. (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. American Museum Novitates 3650, 127.Google Scholar
Ghiselli, F., Milani, L., Scali, V. & Passamonti, M. (2007) The Leptynia hispanica species complex (Insecta Phasmida): polyploidy, parthenogenesis, hybridization and more. Molecular Ecology 16, 42564268.CrossRefGoogle ScholarPubMed
Goudet, J. (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available online at http://www2.unil.ch/popgen/softwares/fstat.htm.Google Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. PNAS 103, 968971.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D. & Ryan, P. (2001) PAST – PAleontological STatisitics software package for education and data analysis. Palaeontologia Electronica 4, 9 pp.Google Scholar
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biology 10, e312.CrossRefGoogle Scholar
Hewitt, G.M. (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London, Series B 359, 183195.CrossRefGoogle ScholarPubMed
Holsinger, K.E., Lewis, P.O. & Dey, D.K. (2002) A Bayesian approach to inferring population structure from dominant markers. Molecular Ecology 11, 11571164.CrossRefGoogle ScholarPubMed
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754755.CrossRefGoogle Scholar
Inward, D., Vogler, A. & Eggleton, P. (2007) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Molecular Phylogenetics and Evolution 44, 953967.CrossRefGoogle ScholarPubMed
Jenkins, T.M., Basten, C.J., Dean, R., Mitchell, S.E., Kresovich, S. & Forschler, B.T. (1999) Matriarchal genetic structure of Reticulitermes (Isoptera: Rhinotermitidae) populations. Sociobiology 33, 239263.Google Scholar
Ketmaier, V., Giusti, F. & Caccone, A. (2006) Molecular phylogeny and historical biogeography of the land snail genus Solatopupa (Pulmonata) in the peri-Tyrrhenian area. Molecular Phylogenetics and Evolution 39, 439451.CrossRefGoogle ScholarPubMed
Korb, J. (2007) Termites. Current Biology 17, R995999.CrossRefGoogle ScholarPubMed
Korb, J. (2008) Termites, hemimetabolous diploid white ants? Frontiers in Zoology 2008, 515.Google Scholar
Kostia, S., Ruohonen-Lehto, M., Väinölä, R. & Varvio, S.L. (2000) Phylogenetic information in inter-SINE and inter-SSR fingerprints of the artiodactyla and evolution of the bov-tA SINE. Heredity 84, 3745.CrossRefGoogle ScholarPubMed
Kutnik, M., Uva, P., Brinkworth, L. & Bagnères, A.G. (2004) Phylogeography of two European Reticulitermes (Isoptera) species: the Iberian refugium. Molecular Ecology 13, 30993113.CrossRefGoogle ScholarPubMed
Luchetti, A. (2005) Identification of a short interspersed repeat in the Reticulitermes lucifugus (Isoptera Rinothermitidae) genome. DNA Sequence 16, 304307.CrossRefGoogle Scholar
Luchetti, A. & Mantovani, B. (2009) Talua SINE Biology in the Genome of the Reticulitermes Subterranean Termites (Isoptera, Rhinotermitidae). Journal of Molecular Evolution 69, 589600.CrossRefGoogle ScholarPubMed
Luchetti, A., Bergamaschi, S., Marini, M. & Mantovani, B. (2004a) Mitochondrial DNA analysis of native European Isoptera: a comparison between Reticulitermes (Rhinotermitidae) and Kalotermes (Kalotermitidae) colonies from Italy and Balkans. Redia 87, 149153.Google Scholar
Luchetti, A., Trenta, M., Mantovani, B. & Marini, M. (2004b) Taxonomy and phylogeny of north mediterranean Reticulitermes termites (Isoptera, Rhinotermitidae): a new insight. Insectes Sociaux 51, 117122.CrossRefGoogle Scholar
Luchetti, A., Marini, M. & Mantovani, M. (2005) Mitochondrial evolutionary rate and speciation in termites: data on European Reticulitermes taxa (Isoptera, Rhinotermitidae). Insectes Sociaux 52, 218221.CrossRefGoogle Scholar
Luchetti, A., Marini, M. & Mantovani, B. (2007) Filling the European gap: Biosystematics of the eusocial system Reticulitermes (Isoptera, Rhinotermitidae) in the Balkanic Peninsula and Aegean area. Molecular Phylogenetics and Evolution 45, 377383.CrossRefGoogle ScholarPubMed
Luscher, M. (1956) Hemmende und fordernde Faktoren bei der Entstehung der Ersatzgeschlechtstiere bei der Termite Kalotermes flavicollis Fabr. Revue Suisse Zoologie 63, 261267.CrossRefGoogle Scholar
Marini, M. & Mantovani, B. (2002) Molecular Relationship among European Samples of Reticulitermes (Isoptera Rhinotermitidae). Molecular Phylogenetics and Evolution 22, 454459.CrossRefGoogle ScholarPubMed
Nishihara, H. & Okada, N. (2008) Retrotransposons: genetic footprints on the evolutionary paths of life. pp. 201225 in Murphy, W.J. (Ed.) Methods in Molecular Biology: Phylogenomics. Totowa, NJ, USA, Humana Press.Google Scholar
Ohshima, K. & Okada, N. (2005) SINEs and LINEs: symbionts of eukaryotic genomes with a common tail. Cytogenetic and Genome Research 110, 475490.CrossRefGoogle ScholarPubMed
Parmakelis, A., Stathi, I., Chatzaki, M., Simaiakis, S., Spanos, L., Louis, C. & Mylonas, M. (2006) Evolution of Mesobuthus gibbosus (Brullé, 1832) (Scorpiones: Buthidae) in the northeastern Mediterranean region. Molecular Ecology 15, 28832894.CrossRefGoogle ScholarPubMed
Perissoratis, C. & Conispoliatis, N. (2003) The impacts of sea-level changes during latest Pleistocene and Holocene times on the morphology of the Ionian and Aegean seas (SE Alpine Europe). Marine Geology 196, 145156.CrossRefGoogle Scholar
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Prota, R. (1962) L'infestazione termitica in Sardegna. Bollettino dell'Istituto di Patologia del Libro XXI, 135.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): a population genetics software for exact test and ecumenicism. Journal of Heredity 86, 248249.CrossRefGoogle Scholar
Rossi, R. & Springhetti, A. (1983) Morphometric research on soldiers of Kalotermes flavicollis Fabr. from Italy. Annali dell'Università di Ferrara - Biologia 3, 4150.Google Scholar
Rozen, S. & Skaletsky, H.J. (2000) Primer3 on the WWW for general users and for biologist programmers. pp. 365386 in Misener, S., Kravetz, S.A. (Eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ, USA, Humana Press.Google Scholar
Schlüter, P.M. & Harris, S.A. (2006) Analysis of multilocus fingerprinting data sets containing missing data. Molecular Ecology Notes 6, 569572.CrossRefGoogle Scholar
Schmitt, T. (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology 2007, 411.Google Scholar
Schmitt, T., Rober, S. & Seitz, A. (2005a) Is the last glaciation the only relevant event for the present genetic population structure of the meadow brown butterfly Maniola jurtina (Lepidoptera: Nymphalidae)? Biological Journal of the Linnean Society 85, 419431.CrossRefGoogle Scholar
Schmitt, T., Varga, Z. & Seitz, A. (2005b) Are Polyommatus hispana and Polyommatus slovacus bivoltine Polyommatus coridon (Lepidoptera: Lycaenidae)? The discriminatory value of genetics in taxonomy. Organisms Diversity and Evolution 5, 297307.CrossRefGoogle Scholar
Sfenthourakis, S. & Legakis, A. (2001) Hotspots of endemic terrestrial invertebrates in southern Greece. Biodiversity and Conservation 10, 13871417.CrossRefGoogle Scholar
Shafer, A.B.A. & Stewart, D.T. (2007) Phylogenetic relationships among Nearctic shrews of the genus Sorex (Insectivora, Soricidae) inferred from combined cytochrome b and inter-SINE fingerprint data using Bayesian analysis. Molecular Phylogenetics and Evolution 44, 192203.CrossRefGoogle ScholarPubMed
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 11141116.CrossRefGoogle Scholar
Spiegelhalter, D.J., Best, N.G., Carlin, B.P. & van der Linde, A. (2002) Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society Series Series B 64, 483689.Google Scholar
Springhetti, A. (1967) Incroci tra reali di alcune popolazioni italiane di Kalotermes flavicollis Fabr. Annali dell'Università di Ferrara - Biologia III, 1117.Google Scholar
Swofford, D.L. (2001) PAUP*-Phylogenetic Analysis Using Parsimony (* and Other Methods), Ver 4b. Sunderland, MA, USA, Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.CrossRefGoogle ScholarPubMed
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
Van Oosterhout, C., Hutchinson, W., Wills, D. & Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
Vasconcelos, T., Horn, A., Lieutier, F., Branco, M. & Kerdelhué, C. (2006) Distribution and population genetic structure of the Mediterranean pine shoot beetle Tomicus destruens in the Iberian Peninsula and Southern France. Agricultural and Forest Entomology 8, 103111.CrossRefGoogle Scholar
Velonà, A., Luchetti, A., Scanabissi, F. & Mantovani, B. (2009) Genetic variability and reproductive modalities in European populations of Triops cancriformis (Crustacea, Branchiopoda, Notostraca). Italian Journal of Zoology 76, 366375.CrossRefGoogle Scholar
Velonà, A., Ghesini, S., Luchetti, A., Marini, M. & Mantovani, B. (2010) Starting from Crete, a phylogenetic re-analysis of the genus Reticulitermes in the Mediterranean area. Molecular Phylogenetics and Evolution 56, 10511058.CrossRefGoogle Scholar
Wahlberg, N. & Saccheri, I. (2007) The effects of Pleistocene glaciations on the phylogeography of Melitaea cinxia (Lepidoptera: Nymphalidae). European Journal of Entomology 104, 675684.CrossRefGoogle Scholar
Zane, L., Bargelloni, L. & Patarnello, T. (2002) Strategies for microsatellite isolation: a review. Molecular Ecology 11, 116.CrossRefGoogle ScholarPubMed
Žurovcová, M., Havelca, J., Stary, P., Vĕchtová, P., Chundelová, D., Jarošová, A. & Kučerová, L. (2010) ‘DNA barcoding’ is of limited value for identifying adelgids (Hemiptera: Adelgidae) but supports traditional morphological taxonomy. European Journal of Entomology 107, 147156.CrossRefGoogle Scholar