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An American termite in Paris: temporal colony dynamics

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Abstract

Termites of the genus Reticulitermes are widespread invaders, particularly in urban habitats. Their cryptic and subterranean lifestyle makes them difficult to detect, and we know little about their colony dynamics over time. In this study we examined the persistence of Reticulitermes flavipes (Kollar) colonies in the city of Paris over a period of 15 years. The aim was (1) to define the boundaries of colonies sampled within the same four areas over two sampling periods, (2) to determine whether the colonies identified during the first sampling period persisted to the second sampling period, and (3) to compare the results obtained when colonies were delineated using a standard population genetic approach versus a Bayesian clustering method that combined both spatial and genetic information. Herein, colony delineations were inferred from genetic differences at nine microsatellite loci and one mitochondrial locus. Four of the 18 identified colonies did not show significant differences in their genotype distributions between the two sampling periods. While allelic richness was low, making it hard to reliably distinguish colony family type, most colonies appeared to retain the same breeding structure over time. These large and expansive colonies showed an important ability to fuse (39% were mixed-family colonies), contained hundreds of reproductives and displayed evidence of isolation-by-distance, suggesting budding dispersal. These traits, which favor colony persistence over time, present a challenge for pest control efforts, which apply treatment locally. The other colonies showed significant differences, but we cannot exclude the possibility that their genotype distributions simply changed over time.

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References

  • Aluko GA, Husseneder C (2007) Colony dynamics of the formosan subterranean termite in a frequently disturbed urban landscape. J Econ Entomol 100:1037–1046

    Article  PubMed  Google Scholar 

  • Arango RA, Marschalek DA, Green F III et al (2015) Genetic analysis of termite colonies in Wisconsin. Environ Entomol. doi:10.1093/ee/nvv023

    PubMed  Google Scholar 

  • Balkenhol N, Fortin M-J (2015) Basics of study design: sampling landscape heterogeneity and genetic variation for landscape genetic studies. In: Balkenhol N, Cushman SA, Storfer AT, Waits LP (eds) Landscape genetics: concepts, methods, applications. Wiley, Chichester, pp 58–76

    Chapter  Google Scholar 

  • Bankhead-Dronnet S, Perdereau E, Kutnik M et al (2015) Spatial structuring of the population genetics of a European subterranean termite species. Ecol Evol. doi:10.1002/ece3.1566

    PubMed  PubMed Central  Google Scholar 

  • Buchli HR (1958) L’origine des castes et les potentialités ontogéniques des termites européens du genre Reticulitermes (Holmgren). In: Annales des Sciences Naturelles vol 12, pp 249–263

  • Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243. doi:10.1007/s002650000304

    Article  Google Scholar 

  • Caron R (2003) Arrêté relatif à la protection des acquéreurs et des propriétaires contre les termites et autres xylophages. Recueil des actes administratifs de la ville de Paris, Paris

    Google Scholar 

  • Chouvenc T, Scheffrahn RH, Su N-Y (2016) Establishment and spread of two invasive subterranean termite species (Coptotermes formosanus and C. gestroi; Isoptera: Rhinotermitidae) in metropolitan Southeastern Florida (1990–2015). Fla Entomol 99:187–191. doi:10.1653/024.099.0205

    Article  Google Scholar 

  • DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441. doi:10.1046/j.1365-294X.2003.02065.x

    Article  PubMed  Google Scholar 

  • DeHeer CJ, Vargo EL (2008) Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the termite Reticulitermes flavipes. Insectes Soc 55:190–199. doi:10.1007/s00040-008-0999-0

    Article  Google Scholar 

  • DeHeer CJ, Kutnik M, Vargo EL, Bagnères A-G (2005) The breeding system and population structure of the termite Reticulitermes grassei in Southwestern France. Heredity 95:408–415. doi:10.1038/sj.hdy.6800744

    Article  CAS  PubMed  Google Scholar 

  • Dronnet S, Ohresser M, Vargo EL et al (2002) Colony studies of the subterranean termite, Reticulitermes santonensis Feytaud, in the city of Paris. In: Proceedings of the 4th International Conference on Urban Pests, pp 7–10

  • 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. doi:10.1111/j.1471-8286.2004.00600.x

    Article  CAS  Google Scholar 

  • Dronnet S, Chapuisat M, Vargo EL et al (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol Ecol 14:1311–1320. doi:10.1111/j.1365-294X.2005.02508.x

    Article  CAS  PubMed  Google Scholar 

  • Dronnet S, Lohou C, Christidès J-P, Bagnères A-G (2006) Cuticular hydrocarbon composition reflects genetic relationship among colonies of the introduced termite Reticulitermes santonensis (Feytaud). J Chem Ecol 32:1027–1042. doi:10.1007/s10886-006-9043-x

    Article  CAS  PubMed  Google Scholar 

  • Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474. doi:10.1146/annurev-ento-120811-153554

    Article  CAS  PubMed  Google Scholar 

  • Frantz AC, Cellina S, Krier A et al (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505. doi:10.1111/j.1365-2664.2008.01606.x

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Lausanne University, Lausanne, Switzerland. http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 13 Dec 2016

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005a) A spatial statistical model for landscape genetics. Genetics 170:1261–1280. doi:10.1534/genetics.104.033803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005b) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. doi:10.1111/j.1471-8286.2005.01031.x

    Article  CAS  Google Scholar 

  • Guillot G, Lebois R, Coulon A, Frantz A (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756. doi:10.1111/j.1365-294X.2009.04410.x

    Article  PubMed  Google Scholar 

  • Guillot G, Renaud S, Ledevin R et al (2012) A unifying model for the analysis of phenotypic, genetic, and geographic data. Syst Biol 61:897–911. doi:10.1093/sysbio/sys038

    Article  PubMed  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16

    Article  CAS  PubMed  Google Scholar 

  • Holzer B, Keller L, Chapuisat M (2009) Genetic clusters and sex-biased gene flow in a unicolonial Formica ant. BMC Evol Biol 9:6–69. doi:10.1186/1471-2148-9-69

    Article  Google Scholar 

  • Husseneder C, Messenger MT, Su N et al (2005) Colony social organization and population genetic structure of an introduced population of Formosan subterranean termite from New Orleans, Louisiana. J Econ Entomol 98:1421–1434

    Article  CAS  PubMed  Google Scholar 

  • Husseneder C, Simms DM, Riegel C (2007) Evaluation of treatment success and patterns of reinfestation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 100:1370–1380

    Article  PubMed  Google Scholar 

  • Husseneder C, Powell JE, Grace JK et al (2008) Worker size in the Formosan subterranean termite in relation to colony breeding structure as inferred from molecular markers. Environ Entomol 37:400–408

    Article  PubMed  Google Scholar 

  • Husseneder C, Simms DM, Delatte JR et al (2012) Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus. Biol Invasions 14:419–437. doi:10.1007/s10530-011-0087-7

    Article  Google Scholar 

  • Leniaud L, Pichon A, Uva P, Bagnères A-G (2009) Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bull Entomol Res 99:1–10. doi:10.1017/S0007485308006032

    Article  CAS  PubMed  Google Scholar 

  • Lohou C, Burban G, Clément J-L et al (1997) Protection des arbres d’alignement contre les Termites souterrains: L’expérience menée à Paris. Phytoma 492:42–44

    Google Scholar 

  • Majid AHA, Ahmad AH (2015) Define colony number of subterranean termites Coptotermes gestroi (Isoptera: Rhinotermitidae) in selected infested structures. Sains Malays 44:211–216

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220

    CAS  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. doi:10.1006/mpev.2000.0790

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia university press, New York

    Google Scholar 

  • Nobre T, Nunes L, Bignell DE (2008) Colony interactions in Reticulitermes grassei population assessed by molecular genetic methods. Insectes Soc 55:66–73. doi:10.1007/s00040-007-0971-4

    Article  Google Scholar 

  • Parman V, Vargo EL (2010) Colony-level effects of imidacloprid in subterranean termites (Isoptera: Rhinotermitidae). J Econ Entomol 103:791–798. doi:10.1603/EC09386

    Article  CAS  PubMed  Google Scholar 

  • Paulmier I, Vauchot B, Pruvost A et al (1997) Evaluation of two populations of Reticulitermes santonensis De Feytaud (Isoptera) by triple mark-recapture procedure. In: 28th annual meeting of the international group of wood preservation. Whistler, pp 25–30

  • Perdereau E, Bagnères A-G, Dupont S, Dedeine F (2010) High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insectes Soc 57:393–402. doi:10.1007/s00040-010-0096-z

    Article  Google Scholar 

  • Perdereau E, Bagnères A-G, Bankhead-Dronnet S et al (2013a) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol Ecol 22:1105–1119. doi:10.1111/mec.12140

    Article  CAS  PubMed  Google Scholar 

  • Perdereau E, Velona A, Dupont S et al (2013b) Colony breeding structure of the invasive termite Reticulitermes urbis (Isoptera: Rhinotermitidae). J Econ Entomol 106:2216–2224

    Article  PubMed  Google Scholar 

  • Perdereau E, Bagnères A-G, Vargo EL et al (2015) Relationship between invasion success and colony breeding structure in a subterranean termite. Mol Ecol 24:2125–2142. doi:10.1111/mec.13094

    Article  CAS  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evol Int J org Evol 43:258–275

    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 N (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375. doi:10.1146/annurev-ento-120710-100634

    Article  CAS  PubMed  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. doi:10.1093/aesa/87.6.651

    Article  CAS  Google Scholar 

  • Su N-Y, Scheffrahn RH (1990) Economically important termites in the United States and their control. Sociobiology 17:77–94

    Google Scholar 

  • Thorne BL, Traniello JFA, Adams ES, 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. Ethol Ecol Evol 11:149–169

    Article  Google Scholar 

  • Tonini F, Hochmair HH, Scheffrahn RH (2013) Simulating the spread of an invasive termite in an urban environment using a stochastic individual-based model. Environ Entomol 42:412–423

    Article  PubMed  Google Scholar 

  • Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–820

    Article  CAS  PubMed  Google Scholar 

  • Vargo EL (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. Environ Entomol 32:1271–1282

    Article  Google Scholar 

  • Vargo EL (2003b) Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evol Int J org Evol 57:2805–2818

    Article  CAS  Google Scholar 

  • Vargo EL (2014) 11 Molecular ecology meets urban entomology: how molecular biology is changing urban pest management. In: Dhang P (ed) Urban insect pests: sustainable management strategies. CABI, p 166

  • Vargo EL, Carlson JR (2006) Comparative study of breeding systems of sympatric subterranean termites (Reticulitermes flavipes and R. hageni) in central North Carolina using two classes of molecular genetic markers. Environ Entomol 35:173–187. doi:10.1603/0046-225X-35.1.173

    Article  Google Scholar 

  • Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403. doi:10.1146/annurev.ento.54.110807.090443

    Article  CAS  PubMed  Google Scholar 

  • Vargo EL, Parman V (2012) Effect of fipronil on subterranean termite colonies (Isoptera: Rhinotermitidae) in the field. J Econ Entomol 105:523–532

    Article  CAS  PubMed  Google Scholar 

  • Vargo EL, Husseneder C, Grace JK (2003) Colony and population genetic structure of the Formosan subterranean termite, Coptotermes formosanus, in Japan. Mol Ecol 12:2599–2608. doi:10.1046/j.1365-294X.2003.01938.x

    Article  CAS  PubMed  Google Scholar 

  • Vargo EL, Juba TR, DeHeer CJ (2006) Relative abundance and comparative breeding structure of subterranean termite colonies (Reticulitermes flavipes. Reticulitermes hageni, Reticulitermes virginicus, and Coptotermes formosanus) in a South Carolina lowcountry site as revealed by molecula. Ann Entomol Soc Am 99:1101–1109

    Article  Google Scholar 

  • Vargo EL, Leniaud L, Swoboda LE et al (2013) Clinal variation in colony breeding structure and level of inbreeding in the subterranean termites Reticulitermes flavipes and R. grassei. Mol Ecol 22:1447–1462. doi:10.1111/mec.12166

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J org Evol 38:1358–1370

    CAS  Google Scholar 

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Acknowledgements

This study is a part of G. Baudouin’s PhD research. We are grateful to Tony Dié and Matthieu Vachon of Pharmabois Company for providing some of the 2016 samples. We also wish to thank Claude Marès and Sylvain Genty of Paris City Hall for sharing their knowledge on termite infestations in the city and providing access to infested buildings. We wish to thank J. Pearce for her English editing services. This work was funded by a contract to A-G Bagnères between the French National Center for Scientific Research (CNRS) and the city of Paris (Direction du Logement et de l’Habitat).

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Correspondence to Anne-Geneviève Bagnères.

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Baudouin, G., Dedeine, F., Bech, N. et al. An American termite in Paris: temporal colony dynamics. Genetica 145, 491–502 (2017). https://doi.org/10.1007/s10709-017-9991-9

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