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Genetic diversity and invasion history of the European subterranean termite Reticulitermes urbis (Blattodea, Termitoidae, Rhinotermitidae)

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Abstract

Biological invasions are among key factors of ecological changes, and social insects appear as highly successful invasive animals. Subterranean termites of the holarctic genus Reticulitermes are present in Europe with six native and one invasive (the nearctic R. flavipes) species. The species R. urbis shows a disjunct distribution in the Western Balkans, Eastern Italy and Southern France. Previous molecular and population genetics data suggested that the taxon originated from the Balkans, and that Italian and French populations are invasive, but it is still unknown how many introduction events occurred and from which Balkan source populations. To address these questions, a population genetics analysis was performed on a larger sampling than previous studies, using mitochondrial cytochrome oxidase II and 6 microsatellite markers on 47 colonies collected across the whole distribution area. Mitochondrial analysis confirmed the presence of two major lineages where colonies from Balkans, Italy, and France intermingle. Similarly, microsatellite loci analysis indicated the presence of two genetic clusters, though not corresponding to the two mitochondrial clades, each including colonies from the three sampled areas and with individuals showing mixed cluster membership. Overall, French and Italian populations showed indications of bottleneck (reduced genetic diversity and change of allele frequencies) and do not appear genetically differentiated from the Balkan population. Results presented here support a history of multiple introductions in Italy and France, in a scenario consistent with continuous exchanges between native and invasive areas, as expected along human trades routes.

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References

  • Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190

    Article  Google Scholar 

  • Ascunce MS, Yang CC, Oakey J et al (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068

    Article  PubMed  CAS  Google Scholar 

  • Astour MC (1985) Ancient Greek Civilization in Southern Italy. J Aesthet Educ 19:23–37

    Article  Google Scholar 

  • Austin JW, Szalanski AL, Uva P, Bagnères A-G, Kence A (2002) A comparative genetic analysis of the subterranean termite genus Reticulitermes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 95:753–760

    Article  CAS  Google Scholar 

  • Bagnères A-G, Uva P, Clément J-L (2003) Description d’une nouvelle espèce de Termite: Reticulitermes urbis n.sp. (Isopt., Rhinotermitidae). Bull Soc Entomol Fr 108:433–435

    Article  Google Scholar 

  • Bignell DE, Eggleton P (2000) Termites in ecosystems. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 363–387

    Chapter  Google Scholar 

  • Buczkowski G, Bertelsmeier C (2016) Invasive termites in a changing climate: a global perspective. Ecol Evol 7:974–985

    Article  Google Scholar 

  • Buttermore RE (1997) Observations at successful Bombus terrestris (L) (Hymenoptera: Apidae) colonies in southern Tasmania. Aust J Entomol 36:251–254

    Article  Google Scholar 

  • Caldera EJ, Ross KG, DeHeer CJ, Shoemaker DD (2008) Putative native source of the invasive fire ant Solenopsis invicta in the USA. Biol Invasions 10:1457–1479

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  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. Mol Phylogenet Evol 94:778–790

    Article  PubMed  Google Scholar 

  • Dlugosh KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 7:431–449

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Dronnet S, Bagnères A-G, Juba TR, Vargo EL (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol Ecol Notes 4:127–129

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol Notes 14:2611–2620

    Article  CAS  Google Scholar 

  • Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474

    Article  PubMed  CAS  Google Scholar 

  • Ferrari R, Ghesini S, Marini M (2011) Reticulitermes urbis in Bagnacavallo (Ravenna, Northern Italy): a 15-year experience in termite control. J Entomol Acarol Res Ser II 43:287–290

    Article  Google Scholar 

  • Ghesini S, Marini M (2012) New data on Reticulitermes urbis and Reticulitermes lucifugus in Italy: are they both native species? Bull Insectol 65:301–310

    Google Scholar 

  • Ghesini S, Marini M (2015) Description of a new termite species from Cyprus and the Aegean area: Reticulitermes aegeus sp. nov. Bull Insectol 68:207–210

    Google Scholar 

  • Ghesini S, Messenger MT, Pilon N, Marini M (2010) First report of Reticulitermes flavipes (Isoptera: Rhinotermitidae) in Italy. Fla Entomol 93:327–328

    Article  Google Scholar 

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

    Google Scholar 

  • Hagenblad J, Hülskötter J, Acharya KP et al (2015) Low genetic diversity despite multiple introductions of the invasive plant species Impatiens glandulifera in Europe. BMC Genet 16:103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holt JA, Lepage M (2000) Termites and soil properties. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 389–407

    Chapter  Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Jeffreys E, Haldon J, Cormack R (2008) The Oxford Handbook of Byzantine Studies. Oxford University Press, New York

    Google Scholar 

  • Jenkins TM, Dean RE, Verkerk R, Forschler BT (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

    Article  PubMed  CAS  Google Scholar 

  • Kinziger AP, Nakamoto RJ, Anderson EC, Harvey BC (2011) Small founding number and low genetic diversity in an introduced species exhibiting limited invasion success (speckled dace, Rhinichthys osculus). Ecol Evol 1:73–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Kutnik M, Uva P, Brinkworth L, Bagnères A-G (2004) Phylogeography of two European Reticulitermes (Isoptera) species: the Iberian refugium. Mol Ecol 13:3099–3113

    Article  PubMed  CAS  Google Scholar 

  • Lander TA, Klein EK, Oddou-Muratorio S, Candau JN, Gidoin C, Chalon A, Roig A, Fallour D, Auger-Rozenberg MA, Boivin T (2014) Reconstruction of a windborne insect invasion using a particle dispersal model, historical wind data, and Bayesian analysis of genetic data. Ecol Evol 4:4609–4625

    Article  PubMed  PubMed Central  Google Scholar 

  • Lefebvre T, Chaline N, Limousin D, Dupont S, Bagnères A-G (2008) From speciation to introgressive hybridization: the phylogeographic structure of an island subspecies of termite, Reticulitermes lucifugus corsicus. BMC Evol Biol 8:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leniaud L, Dedeine F, Pichon A, Dupont S, Bagnères A-G (2009a) Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae). Biol Invasions 12:1389–1402

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  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 Soc 51:117–122

    Article  Google 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. Mol Phylogenet Evol 45:377–383

    Article  PubMed  CAS  Google Scholar 

  • Luchetti A, Scicchitano V, Mantovani B (2013a) Origin and evolution of the Italian subterranean termite Reticulitermes lucifugus (Blattodea, Termitoidae, Rhinotermitidae). Bull Entomol Res 103:734–741

    Article  PubMed  CAS  Google Scholar 

  • Luchetti A, Velonà A, Mueller M, Mantovani B (2013b) Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae). Insectes Soc 60:203–211

    Article  Google Scholar 

  • Marini M, Mantovani B (2002) Molecular relationship among European samples of Reticulitermes (Isoptera, Rhinotermitidae). Mol Phylogenet Evol 22:454–459

    Article  PubMed  CAS  Google Scholar 

  • Mattucci F, Oliveira R, Lyons LA, Alves PC, Randi E (2016) European wildcat populations are subdivided into five main biogeographic groups: consequences of Pleistocene climate changes or recent anthropogenic fragmentation? Ecol Evol 6:3–22

    Article  PubMed  Google Scholar 

  • Miura T, Roisin Y, 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

    Article  PubMed  CAS  Google Scholar 

  • Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142

    Article  Google Scholar 

  • Muirhead JR, Gray DK, Kelly DW et al (2008) Identifying the source of species invasions: sampling intensity vs genetic diversity. Mol Ecol 17:1020–1035

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504

    Article  PubMed  Google Scholar 

  • Perdereau E, Dedeine F, Christidès J-P, Dupont S, Bagnères A-G (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biol Invasions 13:1457–1470

    Article  Google Scholar 

  • Perdereau E, Bagnéres A-G, Bankhead-Dronnet S, Dupont S, Zimmermann M, Vargo EL, Dedeine F (2013a) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol Ecol 22:1105–1119

    Article  PubMed  CAS  Google Scholar 

  • Perdereau E, Velonà A, Dupont S, Labedan M, Luchetti A, Mantovani B, Bagnères A-G (2013b) Colony breeding structure of the invasive termite Reticuliterme urbis (Isoptera: Rhinotermitidae). J Econ Entomol 106:2216–2224

    Article  PubMed  Google Scholar 

  • Perdereau E, Bagnères A-G, Vargo EL, Xu Y, Labadie P, Dupont S, Dedeine F (2015) Relationship between invasion success and colony breeding structure in a subterranean termite. Mol Ecol 24:2125–2142

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Rust MK, Su NY (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375

    Article  PubMed  CAS  Google Scholar 

  • Sarnat EM, Fischer G, Guénard B, Economo EP (2015) Introduced Pheidole of the world: taxonomy, biology and distribution. Zookeys 543:1–109

    Article  Google Scholar 

  • Schmitt T, Seitz A (2001) Allozyme variation in Polyommatus coridon (Lepidoptera: Lycaenidae): identification of ice-age refugia and reconstruction of post-glacial expansion. J Biogeogr 28:1129–1136

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A et al (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

    Article  CAS  Google Scholar 

  • Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol Ecol 9:1517–1528

    Article  PubMed  CAS  Google Scholar 

  • Su NY (2002) Novel technologies for subterranean termite control. Sociobiology 40:95–101

    Google Scholar 

  • Su NY, Scheffrahn RH (2000) Termites as pests of buildings. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 437–453

    Chapter  Google Scholar 

  • Sugimoto A, Bignell DE, MacDonald JA (2000) Global impact of termites on the carbon cycle and atmospheric trace gases. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 409–435

    Chapter  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    PubMed  PubMed Central  CAS  Google Scholar 

  • Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conserv Biol 17:48–58

    Article  Google Scholar 

  • Uva P, Clément J-L, Austin JW, Aubert J, Zaffagnini V, Quintana A, Bagneres A-G (2004) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Mol Phylogenet Evol 30:344–353

    Article  PubMed  CAS  Google Scholar 

  • Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–829

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google 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. Mol Phylogenet Evol 56:1051–1058

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work has been supported by Canziani and RFO-UNIBO funding to AL and BM. Authors wish to thank Francesco Nicassio and Mario Marini for the help in collecting samples. Authors are grateful to two anonymous Reviewers, whose comment and suggestions greatly improved the manuscript.

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Correspondence to Andrea Luchetti.

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Scicchitano, V., Dedeine, F., Bagnères, AG. et al. Genetic diversity and invasion history of the European subterranean termite Reticulitermes urbis (Blattodea, Termitoidae, Rhinotermitidae). Biol Invasions 20, 33–44 (2018). https://doi.org/10.1007/s10530-017-1510-5

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