Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-22T18:40:54.889Z Has data issue: false hasContentIssue false

Origin and evolution of the Italian subterranean termite Reticulitermes lucifugus (Blattodea, Termitoidae, Rhinotermitidae)

Published online by Cambridge University Press:  24 July 2013

A. Luchetti*
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3–40126 Bologna, Italy
V. Scicchitano
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3–40126 Bologna, Italy
B. Mantovani
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3–40126 Bologna, Italy
*
*Author for correspondence Phone: +390512094173 Fax: +390512094286 E-mail: [email protected]

Abstract

The Holarctic genus Reticulitermes shows seven species within the Mediterranean Basin. While phylogeny and systematics at continental level has been deeply investigated, a few studies concentrated on local ranges. To gain a clearer picture of the diversity and evolution of the Italian species Reticulitermes lucifugus, we analyzed the mitochondrial cytochrome oxidase II (COII) gene marker in newly collected colonies across the Peninsula. Data were gathered with all R. lucifugus sequences available from previous studies; COII sequences of the closely related Iberian taxa were also added to the data set. Maximum-likelihood, median-joining and statistical parsimony network elaborations on the resulting 119 colonies all agreed in indicating that: (i) the Sardo-Corsican subspecies R. lucifugus corsicus, strictly related to Southern Italian populations (including the Sicilian ones), is phylogenetically closer to the Iberian Reticulitermes grassei; and (ii) R. lucifugus lucifugus peninsular populations are structured into three clusters. The phylogenetic relationships and the biogeography of extant taxa suggest a scenario in which R. lucifugus ancestors colonized the Italian region through the Sardo-Corsican microplate during its Oligocene-Miocene anticlockwise rotation. Moreover, well after the colonization took place, northward range expansion might have produced the presently observed genetic diversity, as inferred from haplotype and nucleotide diversity estimates. On the whole, this study highlights the evolution of Italian Reticulitermes taxa and supports the importance of a wide taxon sampling especially when dealing with organisms easily dispersed by human activities.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.Google Scholar
Austin, J.W., Szalanski, A.L., Scheffrahn, R.H., Messenger, M.T., Dronnet, S. & Bagneres, A.-G. (2005) Genetic evidendence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Annals of the Entomological Society of America 98, 395401.Google Scholar
Bagnères, A.-G., Uva, P. & CléLment, J.-L. (2003) Description d'une nouvelle espèce de termite: Reticulitermes urbis n. sp. (Isopt., Rhinotermitidae). Bulletin de la Société Entomologique de France 108, 434436.Google Scholar
Bandelt, H.-J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.CrossRefGoogle ScholarPubMed
Bidegaray-Batista, L. & Arnedo, M.A. (2011) Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders. BMC Evolutionary Biology 11, 317.Google Scholar
Clément, J.L., Bagnères, A.-G., Uva, P., Wilfert, L., Quintana, A., Rehinard, J. & Dronnet, S. (2001) Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insectes Sociaux 48, 202215.Google Scholar
Clement, M., Posada, D. & Crandall, K. A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.CrossRefGoogle ScholarPubMed
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
Evans, T.A. (2011) Invasive termites. pp. 321347in Bignell, D.E., Roisin, Y. & Lo, N. (Eds) Biology of Termites: A Modern Synthesis. Dordrecht, Springer.Google Scholar
Ghesini, S. & Marini, M. (2012 a) Morphology and phylogeny of Reticulitermes sp. (Isoptera, Rhinotermitidae) from Cyprus. Bulletin of Entomological Research 102, 672681.Google Scholar
Ghesini, S. & Marini, M. (2012 b) New data on Reticulitermes urbis and Reticulitermes lucifugus in Italy: are they both native species? Bulletin of Insectology 65, 301310.Google Scholar
Hewitt, G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58, 247276.Google Scholar
Jeffery, S., Gardi, C., Jones, A., Montanarella, L., Marmo, L., Miko, L., Ritz, K., Peres, G., Römbke, J. & van der Putten, W.H. (Eds) (2010) European Atlas of Soil Biodiversity. European Commission, Luxembourg, Publications Office of the European Union.Google Scholar
Jenkins, T.M., Dean, R.E., Verkerk, R. & 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. Molecular Phylogenetics and Evolution 20, 286293.Google Scholar
Kutnik, M., Uva, P., Brinkworth, L. & Bagnères, A.-G. (2004) Phylogeography of two European Reticulitermes species: the Iberian refugium. Molecular Ecology 13, 30993113.Google Scholar
Lash, J. (1952) A new species of Reticulitermes from Jerusalem, Palestine. American Museum Novitates 1575, 17.Google Scholar
Lefebvre, T., Châline, N., Limousin, D., Dupont, S. & Bagnères, A.-G. (2008) From speciation to introgressive hybridization: the phylogeographic structure on an island subspecies of termite, Reticulitermes lucifugus corsicus. BMC Evolutionary Biology 8, 38.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Leniaud, L., Dedeine, F., Pichon, A., Dupont, S. & Bagnères, A.-G. (2010) Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae). Biological Invasions 12, 13891402.Google Scholar
Luchetti, A., Trenta, M., Mantovani, B. & Marini, M. (2004) Taxonomy and phylogeny of north mediterranean Reticulitermes termites (Isoptera, Rhinotermitidae): a new insight. Insectes Sociaux 51, 117122.CrossRefGoogle Scholar
Luchetti, A., Marini, M. & Mantovani, B. (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 Balkan peninsula and Aegean area. Molecular Phylogenetics and Evolution 45, 377383.Google Scholar
Luchetti, A., Velonà, A., Mueller, M. & Mantovani, B. (2013 a) Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae). Insectes Sociaux 60, 203211.Google Scholar
Luchetti, A., Dedeine, F., Velonà, A. & Mantovani, B. (2013 b) Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera, Kalotermitidae). Molecular Ecology 22, 33913402.Google Scholar
Mansion, G., Rosenbaum, G., Schoenenberger, N., Bacchetta, G., Rossellò, J.A. & Conti, E. (2008) Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the Mediterranean basin by the angiosperm family Araceae. Systematic Biology 57, 269285.Google Scholar
Marini, M. & Mantovani, B. (2002) Molecular relationship among European samples of Reticulitermes (Isoptera, Rhinotermitidae). Molecular Phylogenetics and Evolution 22, 454459.Google Scholar
Meulenkamp, J. & Sissing, W. (2003) Tertiary palaeogeography and tectonostratigraphic evolution of the Northern and Southern Peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeography, Palaeoclimatology, Palaeoecology 196, 209228.Google Scholar
Perdereau, E., Bagnères, A.-G., Bankhead-Dronnet, S., Dupont, S., Zimmermann, M., Vargo, E.L. & Dedeine, F. (2013) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Molecular Ecology 22, 11051119.Google Scholar
Rosenbaum, G., Lister, G.S. & Duboz, C. (2002) Reconstruction of the tectonic evolution of the western Mediterranean since the Oligocene. Journal of the Virtual Explorer 8, 107130.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619633.CrossRefGoogle ScholarPubMed
Uva, P., Clément, J.L., Austin, J.W., Aubert, J., Zaffagnini, V., Quintana, A. & Bagnères, A.-G. (2004 a) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Molecular Phylogenetics and Evolution 30, 344353.Google Scholar
Uva, P., Clément, J.L. & Bagnères, A.G. (2004 b) Colonial and geographic variations in agonistic behaviour, cuticolar hydrocarbons and mtDNA of Italian populations of Reticulitermes lucifugus (Isoptera, Rhinotermitidae). Insectes Sociaux 51, 163170.Google Scholar
Vargo, E.L. & Husseneder, C. (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annual Review of Entomology 54, 379403.CrossRefGoogle ScholarPubMed
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.Google Scholar
Velona’, A., Luchetti, A., Ghesini, S., Marini, M. & Mantovani, B. (2011) Mitochondrial and nuclear markers highlight the biodiversity of Kalotermes flavicollis (Fabricius, 1793) (Insecta, Isoptera, Kalotermitidae) in the Mediterranean area. Bulletin of Entomological Research 101, 353364.Google Scholar
Webb, T. III & Bartlein, P.J. (1992) Global changes during the last 3 million years: climatic controls and biotic responses. Annual Reviews of Ecology and Systematics 23, 141173.Google Scholar
Supplementary material: File

Luchetti Supplementary Material

Appendix

Download Luchetti Supplementary Material(File)
File 51.7 KB