Skip to main content
Log in

Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae)

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Biological traits and colony structure are difficult to analyze in subterranean termites owing to their cryptic lifestyle and their often elusive breeding system. However, the use of molecular markers in a population genetics framework allows the investigation of such aspects. We present here the colony genetic structures of 12 samples collected along the Italian peninsula of two Reticulitermes species (the native R. lucifugus and the introduced R. urbis) analyzed through nuclear microsatellite markers. Reproductive strategies and colony breeding systems differ between the two species. Secondary reproductives of R. lucifugus, collected in three colonies, are all females; genotyping comparisons between these females and their nest mate workers clearly indicate the presence of asexual queen succession (AQS) events in this species, as observed in the Japanese R. speratus and in the North-American R. virginicus. Two other R. lucifugus colonies have a mixed family genetic pattern, possibly as the result of colony fusion events: accordingly, relatedness estimates indicate the presence of genetically unrelated workers. On the contrary, all R. urbis colonies have a genetic structure compatible with the presence of multiple secondary reproductives, as expected on the basis of previous analyses. Moreover, neotenics’ sex ratio is balanced and their heterozygosity is comparable to that of nest mate workers, suggesting that AQS is lacking in this taxon. The differences observed in such biological traits between the two species are discussed in the light of their invasive potential.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Clément J.L., Bagnères A.G., Uva P., Wilfert L., Quintana A., Rehinard J. and Dronnet S. 2001. Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insect. Soc. 48: 202-215

    Google Scholar 

  • DeHeer C.J. and Vargo E.L. 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

  • DeHeer C.J. and Vargo E.L. 2008. Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the termite Reticulitermes flavipes. Insect. Soc. 55: 190-199

    Google Scholar 

  • DeHeer C.J., Kutnik M., Vargo E.L. and Bagnères A.G. 2005. The breeding system and population structure of the termite Reticulitermes grassei in Southern France. Heredity 95: 408-415

    Google Scholar 

  • Doyle J.J. and Doyle J.L. 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 T.R. and Vargo E.L. 2004. Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol. Ecol. Notes 4: 127-129

  • Dronnet S., Chapuisat M., Vargo E.L., Lohou C. and Bagnères A.G. 2005. Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol. Ecol. 14: 1311-1320

    Google Scholar 

  • Goudet J. 2002. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available at http://www2.unil.ch/popgen/softwares/fstat.htm.

  • Hayashi Y., Kitade O. and Kojima J.I. 2002. Microsatellite loci in the Japanese subterranean termite, Reticulitermes speratus. Mol. Ecol. Notes 2: 518-520

    Google Scholar 

  • Hayashi Y., Kitade O., Gonda M., Kondo T., Miyata H. and Urayama K. 2005. Diverse colony genetic structures in the Japanese subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Sociobiology 46:175-184

    Google Scholar 

  • Helanterä H., Strassmann J.E., Carrilo J. and Queller D.C. 2009. Unicolonial ants: where do they come from what are they and where are they going? Trends Ecol. Evol. 24: 341-349

    Google Scholar 

  • Jones S.C., La Fage J.P. and Howard R.W. 1988. Isopteran sex ratios: phylogenetic trends. Sociobiology 14: 89-118

    Google Scholar 

  • Keller L. 1995. Social life: the paradox of multiple-queen colonies. Trends Ecol. Evol. 10: 355-360

    Google Scholar 

  • Konovalov D.A., Manning C. and Henshaw M.T. 2004. Kingroup: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes 4: 779-782

    Google Scholar 

  • Lainé L.V. and Wright D.J. 2003. The life cycle of Reticulitermes spp. (Isoptera: Rhinotermitidae): what do we know? Bull. Entomol. Res. 93: 267-278

    Google Scholar 

  • Lee A.M., Saether B.E. and Engen S. 2011. Demographic stochasticity, Allee effects, and extinction: the influence of mating system and sex ratio. Am. Nat. 177: 301-313

    Google Scholar 

  • Leniaud L., Pichon A., Uva P. and Bagnères A.G. 2009. Unicoloniality in Reticulitermesurbis: a novel feature in a potentially invasive termite species. Bull. Entomol. Res. 99: 1-10

    Google Scholar 

  • Leniaud L., Dedeine F., Pichon A., Dupont S. and Bagnères A.G. 2010. Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae). Biol. Invasions. 12: 1389-1402

    Google Scholar 

  • Luchetti A., Trenta M., Mantovani B. and Marini M. 2004. Taxonomy and phylogeny of north mediterranean Reticulitermes termites (Isoptera, Rhinotermitidae): a new insight. Insect. Soc. 51: 117-122

    Google Scholar 

  • Luchetti A., Marini M. and Mantovani B. 2007. Filling the European gap: biosystematics of the eusocial system Reticulitermes (Isoptera, Rhinotermitidae) in the Balkanic peninsula and Aegean area. Mol. Phylogenet. Evol. 45: 377-383

    Google Scholar 

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

    Google Scholar 

  • Matsuura K. 2011. Sexual and asexual reproduction in termites. In: Biology of Termites: A Modern Synthesis (Bignell D.E., Roisin Y. and Lo N., Eds). Springer, Dordrecht. pp 321-347

  • Matsuura K., Vargo E.L., Kawatsu K., Labadie P.E., Nakano H., Yashiro T. and Tsuji K. 2009. Queen succession through asexual reproduction in termites. Science 323: 1687

    Google Scholar 

  • Nobre T., Nunes L. and Bignell D.E. 2008. Colony interactions in Reticulitermes grassei population assessed by molecular genetics methods. Insect. Soc. 55: 66-73

    Google Scholar 

  • Peakall R. and Smouse P.E. 2006. GENALEX 6: genetic analysis in Excel. Population genetics software for teaching and research. Mol. Ecol. Notes 6: 288-295

    Google Scholar 

  • Perdereau E., Bagnères A.G., Dupont S. and Dedeine F. 2010. High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insect. Soc. 57: 393-402

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Queller D.C. and Goodnight K.F. 1989. Estimating relatedness using genetic markers. Evolution 43: 258-275

    Google Scholar 

  • Rousset F. 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resources 8: 103-106

    Google Scholar 

  • Schmickl T. and Karsai I. 2010. The interplay of sex ratio, male success and density-independent mortality affects population dynamics. Ecol. Modelling 221: 1089-1097

    Google Scholar 

  • Schmid-Hempel P., Schmid-Hempel R., Brunner P.C., Seeman O.D. and Allen G.R. 2007. Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99: 414-422

    Google Scholar 

  • Thorne B.L., Traniello J.F.A., Adams E.S. and 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

    Google Scholar 

  • Tsutsui N.D. and Suarez A.V. 2003. The colony structure and population biology of invasive ants. Conserv. Biol. 17: 48-58

    Google Scholar 

  • Uva P., Clément J.L. and Bagnères A.G. 2004. Colonial and geographic variations in agonistic behaviour, cuticular hydrocarbons and mtDNA of Italian populations of Reticulitermes lucifugus (Isoptera, Rhinotermitidae). Insect. Soc. 51: 163-170

  • Vargo E.L. 2000. Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol. Ecol. 9: 817-829

    Google Scholar 

  • Vargo E.L. 2003. Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57: 2805-2818

    Google Scholar 

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

    Google Scholar 

  • Vargo E.L. and Husseneder C. 2011. Genetic structure of termite colonies and populations. In: Biology of Termites: A Modern Synthesis (Bignell D.E., Roisin Y. and Lo N., Eds). Springer, Dordrecht. pp 321-347

  • Vargo E.L., Labadie P.E. and Matsuura K. 2012. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc. R. Soc. B 279: 813-819

    Google Scholar 

  • Velonà A., Ghesini S., Luchetti A., Marini M. and Mantovani B. 2010. Starting from Crete, a phylogenetic re-analysis of the genus Reticulitermes in the Mediterranean area. Mol. Phylogenet. Evol. 56: 1051-1058

    Google Scholar 

  • Vieau F.1994. Les stades nymphaux 7 et 8 chez Reticulitermes santonensis Feytaud (Isoptera, Rhinotermitidae). Actes Coll. Insect. Soc. 9: 61–66

  • Zimet M. and Stuart A.M. 1982. Sexual dimorphism in the immature stages of the termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 7: 1-7

    Google Scholar 

Download references

Acknowledgments

This work has been supported by Canziani fund to BM. Authors wish to thank Francesco Nicassio and Nico Radi for colony sampling, and two anonymous reviewers whose suggestions substantially improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Luchetti.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 114 kb)

Supplementary material 2 (PDF 159 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luchetti, A., Velonà, A., Mueller, M. et al. Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae). Insect. Soc. 60, 203–211 (2013). https://doi.org/10.1007/s00040-013-0284-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-013-0284-8

Keywords

Navigation