Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-25T07:08:50.104Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular systematics, biogeography, and colony fusion in the European dry-wood termites Kalotermes spp. (Blattodea, Termitoidae, Kalotermitidae)

Published online by Cambridge University Press:  26 October 2017

V. Scicchitano ,
F. Dedeine ,
B. Mantovani  and
A. Luchetti
V. Scicchitano
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3, 40126 Bologna, Italy
F. Dedeine
Affiliation:
Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS – Université François-Rabelais de Tours, Parc Grandmont, 37200 Tours, France
B. Mantovani
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3, 40126 Bologna, Italy
A. Luchetti*
Affiliation:
Dipartimento di Scienze Biologiche, Geologiche e Ambientali – Università di Bologna, via Selmi 3, 40126 Bologna, Italy
*
*Author for correspondence Tel: +390512094165 Fax: +390512094286 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

European dry-wood termites belong to the genus Kalotermes (Kalotermitidae), one of the two termite genera in Europe. Until the recent description of two new species, Kalotermes italicus in Italy and Kalotermes phoenicae in the eastern Mediterranean area, Kalotermes flavicollis was the only taxon known in this region. The presence of additional entities, suggested by morphological and physiological variation observed in K. flavicollis, was supported by molecular studies revealing four distinct genetic lineages: lineage A, K. flavicollis sensu strictu, from the Aegean area to Italy; lineage B, in Tuscany; lineage SC, in Sardinia and Corsica; lineage SF, in southern France. Lineages A and B may form mixed colonies, suggesting hybridization. To draw a more detailed picture of Kalotermes evolution and biogeography in Europe, we analyzed samples from previously unsampled areas, such as Spain and southern Italy, by means of the highly informative cox1/trnL/cox2 mitochondrial DNA marker. Overall, phylogenetic analyses confirmed previously identified lineages and taxa, but widened the distribution of the lineage SC to the mainland and of the lineage SF to Spain and Portugal. Results further provided evidence for the synonymy between lineage B and K. italicus. Species delimitation analysis suggested that the three K. flavicollis lineages, as well as K. italicus, can be separate taxa. Data also suggest a possible interspecific hybridization between K. italicus and both K. flavicollis lineages A and SC.

Keywords

hybridizationmolecular diversitysocial insectsEuropean species distributiontermitescolony structure
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 4 , August 2018 , pp. 523 - 531
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Aldrich, B.T. & Kambhampati, S. (2009) Preliminary analysis of a hybrid zone between two subspecies of Zootermopsis nevadensis. Insectes Sociaux 56, 439–450.Google Scholar
Becker, G. (1955) Eine Farbmutation mit verändertem ökologischen Verhalten bei Calotermes flavicollis Fabr. (Isoptera). Zeitschrift Fur Angewandte Zoologie 42, 393–404.Google Scholar
Bignell, D.E & Eggleton, P. (2000) Termites in ecosystems. pp. 363–387 in Abe, T., Bignell, D.E. & Higashi, M. (Eds) Termites: Evolution, Sociality, Symbioses, Ecology. Dordrecht, Kluwer Academic Publisher.Google Scholar
Chouvenc, T., Helmick, E.E. & Su, N.-Y. (2015) Hybridization of two major termite invaders as a consequence of human activity. PLoS ONE 10, e0120745.Google Scholar
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1660.Google Scholar
Dedeine, F., Dupont, S., Guyot, S., Matsuura, K., Wang, C., Habibpour, B., Bagnères, A.-G., Mantovani, B. & Luchetti, A. (2016) Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mitochondrial and nuclear loci. Molecular Phylogenetics and Evolution 94, 778–790.Google Scholar
Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.Google Scholar
Drummond, A. J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.Google Scholar
Evans, T.A., Forschler, B.T. & Grace, J.K. (2013) Biology of invasive termites: a worldwide review. Annual Review of Entomology 58, 455–474.Google Scholar
Feldhaar, H., Foitzik, S. & Heinze, J. (2008) Lifelong commitment to the wrong partner: hybridization in ants. Philosophical Transactions of the Royal Society B, Biological Sciences 363, 2891–2899.Google Scholar
Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707–724.Google Scholar
Ghesini, S. & Marini, M. (2013) A dark-necked drywood termite (Isoptera: Kalotermitidae) in Italy: description of Kalotermes italicus sp. nov. Florida Entomologist 96, 200–211.Google Scholar
Ghesini, S. & Marini, M. (2015) Molecular characterization and phylogeny of Kalotermes populations from the Levant, and description of Kalotermes phoeniciae sp. nov. Bulletin of Entomological Research 105, 285–293.Google Scholar
Hart, M.W. & Sunday, J. (2007) Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3, 509–512.CrossRefGoogle ScholarPubMed
Hartke, T.R. & Rosengaus, R.B. (2011) Heterospecific pairing and hybridization between Nasutitermes corniger and N. ephratae. Naturwissenschaften 98, 745–753.Google Scholar
Hendrich, L., Pons, J., Ribera, I. & Balke, M. (2010) Mitochondrial cox1 sequence data reliably uncover patterns of insect diversity but suffer from high lineage-idiosyncratic error rates. PLoS ONE 5, e14448.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, 247–276.Google Scholar
Howard, K.J., Johns, P.M., Breisch, N.L. & Thorne, B.L. (2013) Frequent colony fusions provide opportunities for helpers to become reproductives in the termite Zootermopsis nevadensis. Behavioural Ecology and Sociobiology 67, 1575–1585.Google Scholar
Inward, D.J., Vogler, A.P. & Eggleton, P. (2007) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Molecular Phylogenetics and Evolution 44, 953–967.CrossRefGoogle ScholarPubMed
Johns, P.M., Howard, K.J., Breisch, N.L., Rivera, A. & Thorne, B. (2009) Non-relatives inherit colony resources in a primitive termite. Proceedings of the National Academy of Science USA 106, 17452–17456.CrossRefGoogle Scholar
Korb, J. & Roux, E.A. (2012) Why join a neighbour: fitness consequences of colony fusion in termites. Journal of Evolutionary Biology 25, 2161–2170.Google Scholar
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Lefebvre, T., Châline, N., Limousin, D., Dupont, S. & Bagneres, 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.CrossRefGoogle Scholar
Lefebvre, T., Vargo, E.L., Zimmermann, M., Dupont, S., Kutnik, M. & Bagnéres, A.-G. (2016) Subterranean termite phylogeography reveals multiple postglacial colonization events in southwestern Europe. Ecology and Evolution 6, 5987–6004.CrossRefGoogle ScholarPubMed
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Luchetti, A., Bergamaschi, S., Marini, M. & Mantovani, B. (2004) Mitochondrial DNA analysis of native European Isoptera: a comparison between Reticulitermes (Rhinotermitidae) and Kalotermes (Kalotermitidae) colonies from Italy and Balkans. Redia LXXXVII, 149–153.Google Scholar
Luchetti, A., Dedeine, F., Velonà, A. & Mantovani, B. (2013a) Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera, Kalotermitidae). Molecular Ecology 22, 3391–3402.CrossRefGoogle ScholarPubMed
Luchetti, A., Scicchitano, V. & Mantovani, B. (2013b) Origin and evolution of the Italian subterranean termite Reticulitermes lucifugus (Blattodea, Termitoidae, Rhinotermitidae). Bulletin of Entomological Research 103, 734–741.Google Scholar
Luscher, M. (1956) Hemmende und fordernde Faktoren bei der Entstehung der Ersatzgeschlechtstiere bei der Termite Kalotermes flavicollis Fabr. Revue Suisse Zoologie 63, 261–267.Google Scholar
Maistrello, L., Ocete, R. & López, M.A. (2010) Seasonal trends in the social composition and inside-trunk distribution of Kalotermes flavicollis (Isoptera: Kalotermitidae) colonizing grapevines. Environmental Entomology 39, 295–302.Google Scholar
Monaghan, M.T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D.J.G., Lees, D.C., Ranaivosolo, R., Eggleton, P., Barraclough, T.G. & Vogler, A.P. (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Scicchitano, V., Dedeine, F., Bagnères, A.-G., Luchetti, A. & Mantovani, B. (2017) Genetic diversity and invasion history of the European subterranean termite Reticulitermes urbis (Blattodea, Termitoidae, Rhinotermitidae). Biological Invasions in press (doi: 10.1007/s10530-017-1510-5).Google Scholar
Springhetti, A. (1967) Incroci tra reali di alcune popolazioni italiane di Kalotermes flavicollis Fabr. Annali dell'Università di Ferrara, Biologia III, 11–17.Google Scholar
Tang, C.Q., Humphreys, A.M., Fontaneto, D. & Barraclough, T.G. (2014) Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data. Methods in Ecology and Evolution 5, 1086–1094.Google Scholar
Thompson, G.J., Miller, L.R., Lenz, M. & Crozier, R.H. (2000) Phylogenetic analysis and trait evolution in Australian lineages of drywood termites (Isoptera, Kalotermitidae). Molecular Phylogenetics and Evolution 17, 419–429.Google Scholar
Thorne, B.L., Breisch, N.K & Muscedere, M.L. (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proceedings of the National Academy of Science USA 100, 12808–12813.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, 379–403.Google Scholar
Vargo, E.L. & Husseneder, C. (2011) Genetic structure of termite colonies and populations. pp. 321–347 in Bignell, D., Roisin, Y. & Lo, N. (Eds) Biology of Termites: A Modern Synthesis. Heidelberg, Springer.Google Scholar
Velonà, 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, 353–364.Google Scholar
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Scicchitano et al supplementary material 1

Supplementary Table

Download Scicchitano et al supplementary material 1(PDF)
PDF 22.7 KB