Eur. J. Entomol. 113: 409-414, 2016 | 10.14411/eje.2016.053

Identification of microsatellite markers for a worldwide distributed, highly invasive ant species Tapinoma melanocephalum (Hymenoptera: Formicidae)

Jan ZIMA Jr.1,2, Ophélie LEBRASSEUR3, Michaela BOROVANSKÁ2, Milan JANDA2,4
1 Faculty of Sciences, Department of Zoology, Branišovská 31, 370 05 České Budějovice, Czech Republic; e-mail: zimapanz@seznam.cz
2 Biology Centre CAS, Institute of Entomology, Branišovská 31, 370 05 České Budějovice, Czech Republic; e-mails: michaela.borovanska@seznam.cz, jandamil@gmail.com
3 Palaeo-Genomics and Bio-Archaeological Research Network, Research Laboratory for Archaeology, Dyson Perrins Building, South Parks Road, OX1 3QY, Oxford, United Kingdom; e-mail: ophelie.lebrasseur@arch.ox.ac.uk
4 University of Guanajuato, Department of Biology, Noria Alta sn. Guanajuato, Mexico

Tapinoma melanocephalum is a worldwide distributed, highly invasive ant species. It lives in close association with human societies and its distribution is human-mediated in large measure. The geographical origin of this ant species is unknown, but its introduction in areas previously devoided of its presence can represent a threat to the native biota, act as an agricultural pest or as a pathogen vector. To investigate the genetic structure and phylogeography of this species we identified 12 new polymorphic microsatellite markers, and in addition, we tested and selected 12 ant-universal microsatellites polymorphic in T. melanocephalum. We genotyped 30 individuals from several islands of Micronesia and Papua-New Guinea. All 24 loci exhibited strong homozygosity excess (45-100%, mean = 86%), while the number of alleles per locus reached usual values (2-18, mean = 6.5), resulting in levels of expected heterozygosity much higher than observed. Based on several robust tests, we were able to exclude artefacts such as null alleles and allelic dropout as a possible cause of the observed pattern. Homozygosity excess might be a consequence of founder effect, bottleneck and/or inbreeding. As our sample population was composed of individuals from several distinct localities, the Wahlund effect might have contributed to the increased homozygosity as well. Despite the provisionally observed deviation from the Hardy-Weinberg equilibrium, the newly developed microsatellites will provide an effective tool for future genetic investigations of population structure as well as for the phylogeographic study of T. melanocephalum.

Keywords: Hymenoptera, Formicidae, Tapinoma melanocephalum, microsatellites, invasive species, homozygosity excess

Received: February 18, 2016; Accepted: May 16, 2016; Published online: June 3, 2016

Download citation

References

  1. Appel A.G.J., Na J.P.S. & Lee C.Y. 2004: Temperature and humidity tolerances of the ghost ant, Tapinoma melanocephalum (Hymenoptera: Formicidae). - Sociobiology 44: 89-100.
  2. Bustos X. & Cherix D. 1998: Contribution à la biologie de Tapinoma melanocephalum (Fabricius) (Hymenoptera: Formicidae). - Actes Coll. Insectes Soc. 11: 95-101.
  3. Butler I.A., Siletti K., Oxley P.R. & Kronauer D.J.C. 2014: Conserved microsatellites in ants enable population genetic and colony pedigree studies across a wide range of species. - PloS One 9(9): e107334, 11 pp. Go to original source...
  4. Choe H.C., Lim J.O. & Lee S. 2009: Tapinoma melanocephalum (Fabricius), a new exotic pest in Korea. - J. Asia-Pac. Entomol. 12: 67-69.
  5. Clouse R.M. 2007: The ants of Micronesia (Hymenoptera: Formicidae). - Micronesica 39: 171-275.
  6. Collingwood C.A. 1979: The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica. Vol. 8. Scandinavian Science Press, Klampenborg, 174 pp.
  7. Ekblom R. & Galindo J. 2011: Applications of next generation sequencing in molecular ecology of non-model organisms. - Heredity 107: 1-15. Go to original source...
  8. Frankham R., Ballou J. & Briscoe D. 2008: Introduction to Conservation Genetics. Cambridge University Press, Cambridge, 617 pp.
  9. Gagneux P., Boesch C. & Woodruff D.S. 1997: Microsatellite scoring errors associated with noninvasive genotyping based on nuclear DNA amplified from shed hair. - Mol. Ecol. 6: 861-868. Go to original source...
  10. Harada Y. 1990: Ant pests of the Tapinomini tribe. In Vander Meer R.K., Jaffe K. & Cedeno A. (eds): Applied Myrmecology. A World Perspective. Westview Press, Boulder, pp. 298-315.
  11. Klimes P., Idigel C., Rimandai M., Fayle T.M., Janda M., Weiblen G.D. & Novotný V. 2012: Why are there more arboreal ant species in primary than in secondary tropical forests? - J. Anim. Ecol. 81: 1103-1112. Go to original source...
  12. Kureck I.M., Jongepier E., Nicolai B. & Foitzik S. 2012: No inbreeding depression but increased sexual investment in highly inbred ant colonies. - Mol. Ecol. 21: 5613-5623. Go to original source...
  13. Lebrasseur O.M.M. 2014: Dogs, Chickens and Ants: Investigating the Reliability of Modern Maternal Genetic Data in Retracing Early Dispersals. PhD Thesis, Durham University, 32 pp.
  14. Malausa T., Gilles A., Meglecz E., Blanquart H., Duthoy S., Costedoat C., Dubut V., Pech N., Castagnone-Sereno P., Délye C. et al. 2011: High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. - Mol. Ecol. Resour. 11: 638-644. Go to original source...
  15. Mesak F., Tatarenkov A., Early R.L. & Avise J.C. 2014: Hundreds of SNPs vs. dozens of SSRs: which dataset better characterizes natural clonal lineages in a self-fertilizing fish? - Front. Ecol. Evol. 2: 74. Go to original source...
  16. Moreira D.D.O., Morais V., Vieira-da-Motta O., Campos-Farinha A.E.C. & Tonhasca Jr. A. 2005: Ants as carriers of antibiotic-resistant bacteria in hospitals. - Neotrop. Entomol. 34: 999-1006. Go to original source...
  17. Passera L. 1994: Characteristics of tramp species. In Williams D.F. (ed.): Exotic Ants. Westview Press, Boulder, CO, pp. 23-43.
  18. Peakall R. & Smouse P.E. 2006: GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. - Mol. Ecol. Notes 6: 288-295. Go to original source...
  19. Pearcy M., Hardy O. & Aron S. 2006: Thelytokous parthenogenesis and its consequences on inbreeding in an ant. - Heredity 96: 377-382. Go to original source...
  20. Rousset F. 2008: Genepop ´007: a complete re-implementation of the genepop software for Windows and Linux. - Mol. Ecol. Resour. 8: 103-106. Go to original source...
  21. Sabatti C. & Risch N. 2002: Homozygosity and linkage disequilibrium. - Genetics 160: 1707-1719.
  22. Schlick-Steiner B.C., Arthofer W., Moder K. & Steiner F.M. 2014: Recent insertion/deletion (reINDEL) mutations: increasing awareness to boost molecular-based research in ecology and evolution. - Ecol. Evol. 5: 24-35. Go to original source...
  23. Selkoe K.A. & Toonen R.J. 2006: Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. - Ecol. Lett. 9: 615-629. Go to original source...
  24. Slatkin M. 2008: Linkage disequilibrium - understanding the evolutionary past and mapping the medical future. - Nature Rev. Genet. 9: 477-485. Go to original source...
  25. Smith M.R. 1965: House-infesting ants of the eastern United States. Their recognition, biology, and economic importance. - U.S.D.A. Technol. Bull. 1326: 1-105.
  26. Thurin N. & Aron S. 2009: Sib-mating in the ant Plagiolepis pygmaea: adaptive inbreeding? - J. Evol. Biol. 22: 2481-2487. Go to original source...
  27. Trontti K., Aron S. & Sundstrom L. 2005: Inbreeding and kinship in the ant Plagiolepis pygmaea. - Mol. Ecol. 14: 2007-2015. Go to original source...
  28. Tsutsui N.D. & Suarez A.V. 2003: The colony structure and population biology of invasive ants. - Conserv. Biol. 17: 48-58. Go to original source...
  29. Venkataramaiah G.H. & Rehman P.A. 1989: Ants associated with the mealybugs of coffee. - Indian Coffee 43: 13-14.
  30. Wetterer J.K. 2009: Worldwide spread of the ghost ant, Tapinoma melanocephalum (Hymenoptera: Formicidae). - Myrmecol. News 12: 23-33.
  31. Wen W.J. 2007: The Feeding Behaviour of the Ghost Ants, Tapinoma melanocephalum (Fabricius) and Tapinoma indicum (Forel) (Hymenoptera: Formicidae). Master Thesis, University Sains Malaysia, 154 pp.