Skip to main content
Log in

Sequence comparisons of the internal transcribed spacer region of ribosomal genes support close relationships between parasitic ants and their respective host species (Hymenoptera: Formicidae)

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

Summary

A fragment of the internal transcribed spacer (ITS-1) adjacent to the 5.8S rRNA gene of 20 myrmicine ant species was sequenced. Sequence comparisons were carried out between 11 species of the tribe Leptothoracini, five species of the tribe Tetramoriini, three species of the tribe Solenopsidini and one species of the tribe Myrmicini. Additionally, the formicine antCamponotus ligniperda (tribe Camponotini) was analyzed as an outgroup species. Among all investigated species, the fragment had a variable length of ≈ 230–380 bp with only a few conserved sequence elements. The sequences of this fragment were perfectly identical within four palearctic populations ofLeptothorax acervorum indicating that intraspecific variation is rather low. Within the species of Tetramoriini (includingAnergates atratulus) 94.1% of sequence positions were identical, 95.6% within the species of theLeptothorax s.str.-group and 64.6% within the species of theMyrafant-group. Phylogenetic analysis reveals that the social parasitesHarpagoxenus sublaevis, Doronomyrmex goesswaldi, D. kutteri andD. pacis, Chalepoxenus muellerianus as well asStrongylognathus alpinus andTeleutomyrmex schneideri are most closely related to the groups of their respective host species, which generally confirms the taxonomical classifications of the subfamily Myrmicinae based on morphological criteria. The taxonomical positions of the speciesA. atratulus has as yet been uncertain, however, sequence comparison of the ITS-1 fragment leads to the conclusion thatA. atratulus rather belongs to the tribe Tetramoriini than to the Solenopsidini.

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.

Similar content being viewed by others

References

  • Arnheim, N., 1983. Concerted evolution of multigene families. In:Evolution of Genes and Proteins (M. Nei and R. K. Koehn, eds.), Sinauer, Sunderland, Mass. pp. 38–61.

    Google Scholar 

  • Arnold, M. L., D. D. Shaw and M. Contreras, 1987. Ribosomal RNA-encoding DNA introgression across a narrow hybrid zone between two subspecies of grasshopper.Proc. Natl. Acad. Sci. USA 84:3946–3950.

    Google Scholar 

  • Baur, A., A. Buschinger and F. K. Zimmermann, 1993. Molecular cloning and sequencing of 18S rDNA gene fragments from six different ant species.Ins. Soc. 40:325–335.

    Google Scholar 

  • Bolton, B., 1976. The ant tribe Tetramoriini (Hymenoptera: Formicidae): constituent genera, review of smaller genera and revision ofTriglyphothrix FOREL.Bull. Brit. Mus. nat. Hist. (Ent.) 34:281–379.

    Google Scholar 

  • Buschinger, A., 1987. Biological arguments for a systematic rearrangement of the ant tribe Leptothoracini. In:Chemistry and Biology of Social Insects (J. Eder and H. Rembold, eds.), J. Peperny, München, p. 43.

    Google Scholar 

  • Buschinger, A., 1990. Sympatric speciation and radiative evolution of socially parasitic ants — Heretic hypotheses and their factual background.Z. Zool. Syst. Evolut.-forsch. 28:241–260.

    Google Scholar 

  • Coen, E. S., T. Strachan and G. A. Dover, 1982. Dynamics of concerted evolution of ribosomal DNA and histone gene families in themelanogaster species subgroup ofDrosophila.J. Mol. Biol. 158:17–35.

    PubMed  Google Scholar 

  • Devereux, J., P. Haeberli and O. Smithies, 1984. A comprehensive set of sequence analysis programmes for the VAX.Nucleic Acid Res. 12:387–395.

    PubMed  Google Scholar 

  • Douwes, P. and B. Stille, 1987. The use of enzyme electrophoresis inLeptothorax classification. In:Chemistry and Biology of Social Insects (J. Eder and H. Rembold, eds.), J. Peperny, München, pp. 29–30.

    Google Scholar 

  • Dowling, T. E., C. Moritz and J. Palmer, 1990. Nucleic acids II: Restriction site analysis. In:Molecular Systematics (D. M. Hillis and C. Moritz, eds.), Sinauer, Sunderland, Mass. pp. 250–317.

    Google Scholar 

  • Dover, G. and E. Coen, 1981. Springcleaning ribosomal DNA. A model for multigene evolution?Nature 290:731–732.

    PubMed  Google Scholar 

  • Emery, C., 1909. Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen.Biol Zbl. 29:352–362.

    Google Scholar 

  • Emery, C., 1921-1922. Hymenoptera, fam. Formicidae, subfam. Myrmicinae. In:Genera Insec-torum, no. 174 (P. Wytsman, ed.), Louis Desmet-Verteneul, Brussels. 397 pp.

    Google Scholar 

  • Ettershank, G., 1966. A generic revision of the world Myrmicinae related toSolenopsis andPheidologeton.Aust. J. Zool. 14:73–171.

    Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap.Evolution 39:783–791.

    Google Scholar 

  • Felsenstein, J., 1989. PHYLIP — Phylogeny Inference Package (Version 3.2).Cladistics 5:164–166.

    Google Scholar 

  • Felsenstein, J., 1993. PHYLIP (Phylogeny Inference Package) Version 3.5 c. Dep. of Genetics, University of Washington, Seattle.

  • Fitch, W. M. and E. Margoliash, 1967. Construction of phylogenetic trees.Science 155:279–284.

    PubMed  Google Scholar 

  • Fujiwara, H., Y. Kawata and H. Ishikawa, 1982. Primary structure of the 5.8S rRNA from the silk gland ofBombyx mori.Nucleic Acid Res. 10:2415–2418.

    PubMed  Google Scholar 

  • Gonzales, I. L., C. Chambers, J. L. Gorski, D. Stambolian, R. D. Schmickel and J. E. Sylvester, 1990. Sequence and structure correlation of human ribosomal transcribed spacers.J. Mol. Biol. 212:27–35.

    PubMed  Google Scholar 

  • Heinze, J., 1991. Biochemical studies on the relationship between socially parasitic ants and their hosts.Biochem. Syst. Ecol. 19:195–206.

    Google Scholar 

  • Hillis, D. M. and M. T. Dixon, 1991. Ribosomal DNA: Molecular evolution and phylogenetic inference.Quart. Rev. Biol. 66:411–453.

    PubMed  Google Scholar 

  • Hölldobler, B. and E. O. Wilson, 1990.The Ants. The Belknap Press of Harvard University Press, Cambridge, Mass. 732 pp.

    Google Scholar 

  • Jukes, T. H. and R. C. Cantor, 1969. Evolution of protein molecules. In:Mammalian protein metabolism (H. N. Munoro, ed.), Academic Press, New York. pp. 21–132.

    Google Scholar 

  • Kuperus, W. R. and W. Chapco, 1994. Usefulness of internal transcribed spacer regions of ribosomal DNA in melanopline (Orthoptera: Acrididae) systematics.Ann. Entomol. Soc. Am. 87:751–754.

    Google Scholar 

  • Kutter, H., 1969. Die sozialparasitischen Ameisen der Schweiz.Neujahrsbl. Naturf. Ges. Zürich 1969:1–62.

    Google Scholar 

  • Kutter, H., 1977. Hymenoptera: Formicidae. In:Insecta Helvetica, vol. 6 (W. Sauter, ed.), Schweiz. Ent. Ges., Zürich. 289 pp.

    Google Scholar 

  • Kwok, S. and R. Higuchi, 1989. Avoiding false positives with PCR.Nature 339:237–238.

    PubMed  Google Scholar 

  • Mullis, K. B. and F. Faloona, 1987. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction.Methods Enzymol. 155:335–350.

    PubMed  Google Scholar 

  • Muster, W., K. Boon, A. F. M. van der Sande, H. van Heerikuizen and R. J. Planta, 1990. Functional analysis of transcribed spacers of yeast ribosomal DNA.EMBO J. 9:3989–3996.

    PubMed  Google Scholar 

  • Nazar, R. N., T. O. Sitz and H. Busch, 1976. Sequence homologies in the mammalian 5.8S ribosomal RNA.Biochemistry 15:505–508.

    PubMed  Google Scholar 

  • Pavlakis, G. N., B. R. Jourdan, R. M. Wurst and C. Vournakis, 1979. Sequence and secondary structure ofDrosophila melanogaster 5.8S and 28S rRNAs and of the processing site between them.Nucleic Acid Res. 7:2213–2238.

    PubMed  Google Scholar 

  • Pearson, W. R. and D. J. Lipman, 1988. Improved tools for biological sequence comparison.Proc. Natl. Sci. USA 85:2444–2448.

    Google Scholar 

  • Ritland, C. E., K. Ritland and N. A. Straus, 1993. Variation in the ribosomal internal transcribed spacers (ITS1 and ITS2) among eight taxa of theMimulus guttatus species complex.Mol Biol. Evol. 10:1273–1288.

    PubMed  Google Scholar 

  • Rubin, G. M., 1973. The nucleotide sequence ofSaccharomyces cerevisiae 5.8S ribosomal nucleic acid.J. Biol. Chem. 248:3860–3875.

    PubMed  Google Scholar 

  • Saiki, R. K., S. Scharf, F. Faloona, K. B. Mullis, G. T. Horu, H. A. Erlich and N. Arnheim, 1985. Enzymatic amplification of β-globulin sequences and restriction site analysis for diagnosis of sickle cell anemia.Science 230:1350–1354.

    PubMed  Google Scholar 

  • Saitou, N. and M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees.Mol. Biol. Evol. 4:406–425.

    PubMed  Google Scholar 

  • Sanetra, M., J. Heinze and A. Buschinger, 1994. Enzyme polymorphism in the ant genusTetramorium Mayr and its social parasites.Biochem. Syst. Ecol. 22:753–759.

    Google Scholar 

  • Sambrook, J., E. F Fritsch and T. Maniatis, 1989.Molecular cloning — a Laboratory Manual, Second Edition. Cold Spring Harbour Laboratory Press.

  • Sanger, F., S. Nicklen and M. Coulson, 1977. DNA sequencing with chain terminating inhibitors.Proc. Natl. Acad. Sci. USA 162:5463–5467.

    Google Scholar 

  • Smith, T. F. and M. S. Waterman, 1981. Comparison of bio-sequences.Adv. Appl. Math. 2:482–488.

    Google Scholar 

  • Tautz, D., C. Tautz, D. Webb and G. A. Dover, 1987. Evolutionary divergence of promoters and spacers in the rDNA family of fourDrosophila species. Implications for molecular coevolution in multigene families.J. Mol. Biol. 195:525–542.

    PubMed  Google Scholar 

  • Wesson, D. M., D. K. McLain, J. H. Oliver, J. Piesman and F. H. Collins, 1993. Investigation of the validity of species status ofIxodes dammini (Acari: Ixodidae) using rDNA.Proc. Natl. Acad. Sci. USA 90:10221–10225.

    PubMed  Google Scholar 

  • Wesson, D. M., C. H. Porter and F. H. Collins, 1992. Sequence and secondary structure comparison of the ITS rDNA in Mosquitoes (Diptera: Culicidae).Mol. Phylogen. Evol. 1:253–269.

    Google Scholar 

  • Wheeler, G. C. and J. Wheeler, 1985. A simplified conspectus of the Formicidae.Trans. Am. Entomol. Soc. 111:255–264.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Author who provided the sequence data from his doctoral thesis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baur, A., Sanetra, M., Chalwatzis, N. et al. Sequence comparisons of the internal transcribed spacer region of ribosomal genes support close relationships between parasitic ants and their respective host species (Hymenoptera: Formicidae). Ins. Soc 43, 53–67 (1996). https://doi.org/10.1007/BF01253956

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01253956

Key words

Navigation