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Type: Article
Published: 2007-11-12
Page range: 59–68
Abstract views: 42
PDF downloaded: 2

High nucleotide divergence in a dimorphic parasite with disparate hosts

Department of Zoology, University of Oxford, Oxford, United Kingdom, OX1 3PS, UK
Department of Entomology, Texas A&M University, College Station, TX 77843, USA Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, VA 24061, Blacksburg, VA, USA
Department of Zoology, University of Oxford, Oxford, United Kingdom, OX1 3PS, UK
Department of Entomology, Texas A&M University, College Station, TX 77843, USA Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
Department of Entomology, Texas A&M University, College Station, TX 77843, USA
Strepsiptera Myrmecolacidae Caenocholax fenyesi sensu lato 28S rDNA 18S rDNA

Abstract

Morphologically cryptic male C. fenyesi sensu lato are found parasitic in different ant hosts over a wide geographical range. We use ribosomal DNA (rDNA) primary sequence and predicted rRNA secondary structure to compare between the second expansion segment (D2) of the nuclear large subunit rDNA (28S) and the entire nuclear small subunit rDNA (18S) of the male and the sexually dimorphic, neotenic female of Caenocholax fenyesi waloffi Kathirithamby & Johnston from Los Tuxtlas, Mexico, with that of the morphologically identical male C. f. texensis Kathirithamby & Johnston (Myrmecolacidae) from Texas, USA. In Los Tuxtlas the male C. f. waloffi parasitizes the ant, Dolichoderus bispinosus Olivier, while the female parasitizes the cricket, Macroanaxipha macilenta (Saussure). In Texas, the male C. f. texensis parasitizes the red imported fire ant, Solenopsis invicta Buren. The compared sequences show similar unusual secondary structures in the rRNA variable regions, but with approximately 14% overall divergence between Mexican and Texan specimens (15.5% divergence after correction for multiple substitutions). Our findings open a new opportunity in evolutionary biology to investigate speciation under a mechanism of morphological stasis and high genetic divergence in a unique parasite that is not only profoundly sexually dimorphic but wherein the sexes specialize in entirely different niches (hosts).

References

  1. Altschul, S.F., Gish, W., Miller, E.W., Myers, M. & Lipman, D.J. (1990) Basic local alignmet search tool. Journal of Molecular Biology, 215, 204–410.

    Babcock, C.S. & Heraty, J.M. (2005) Molecular markers distinguishing Encarsia formosa and Encarsia luteola (Hymenoptera: Aphelinidae). Annals of the Entomological Society of America, 93, 738–744.

    Cannone, J. J., Subramanian, S., Schare, M. N., Collett, J. R., D’ Souza, L. M., Du, Y., Feng, B., Lin, N., Medabusi, L. V., Müller, K. M., Pande, N., Sang, Z., Yu, N. & Gutell, R. R. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structural information for ribsomal, intron and other RNAs: correction. BMC Bioinformatics 3, 15.

    Cognato, A.I. (2006) Standard percent DNA sequence difference for insects will not predict species boundaries. Journal of Economic Entomology, 99, 1037-1045.

    Dover, G.A. (1982) A cohesive mode of species evolution. Nature, 299, 111–117.

    Gillespie, J.J. (2004) Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules. Molecular Phylogenetics and Evolution, 33, 936–934.

    Gillespie, J.J., Cannone, J.J., Gutell, R.R. & Cognato, A. (2004) A secondary structural model of the 28S rRNA expansion segments D2 and D3 from rootworms and related leaf beetles (Coleoptera: Chrysomelidae: Galerucinae). Insect Molecular Biology, 13, 495–518.

    Gillespie, J.J., McKenna, C., Yoder, M.J., Gutell, R., Johnston, J.S., Kathirithamby, J. & Cognato, A.I. (2005a) Assessing the odd secondary structural properties of nuclear ribosomal RNA sequences (18S) of the twisted winged parasites (Insecta: Strepsiptera). Insect Molecular Biology, 14, 625-643.

    Gillespie, J.J., Munro, J.B., Heraty, J.M., Yoder, M.J., Owen, A.K. & Carmichael, A.E. (2005b) A secondary structural model of the 18S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution, 22, 1593–1608.

    Gillespie, J.J., Yoder, M.J. & Wharton, R.A. (2005c) Predicted secondary structures for 28S and 18S rRNA from Ichneumonoidea (Insecta: Hymenoptera: Apocrita): Impact on sequence alignment and phylogeny estimation. Journal of Molecular Evolution, 61, 114–137.

    Gillespie, J.J., Johnston, J.S., Cannone, J.J. & Gutell, R.R., (2006) Characteristics of the Nuclear (18S, 5.8S, 28S, and 5S) and mitochondrial (16S and 12S) RNA genes of Apis mellifera (Insecta: Hymenoptera): Structure, organization and retrotransponsable elements. Insect Molecular Biology, 15, 657-686.

    Halbert, N.R., Ross, L.D., Kathirithamby, J., Woolley, J.B., Saff, R.R. & Johnston, J.S. (2001) Phylogenetic analysis as a means of species identification within Myrmecolacidae (Insecta: Strepsiptera). Tijdschrift voor Entomologie, 144, 179–186.

    Hunter, M.S., Woolley, J.B. (2001) Evolutionary and behavioural ecology of heteronomous Aphelinid parasitoids. Annual Review of Entomology 46, 251-290.

    Hayat, M. (1985) Family Aphelinidae. in B. R. Subba Rao, & H. Hayat, (eds), The Chalcidoidea of India and the Adjacent Countries. Reviews of families and keys to families and genera, Part I. Oriental Insects, 19, 163–310.

    Huyse, T., Poulin, R. & Theron, A. (2005) Speciation in parasites: a population genetics approach. Trends in Parasitology, 21, 469–474.

    Jukes, T.H. & Cantor, C.R. (1969) Evolution in protein molecules. pp. 21–123 in H. N. Munroe (ed.). Mammalian Protein Metabolism. Academic Press, New York.

    Kathirithamby, J. (2005) Further Homage to Santa Rosalia: Discovery at last of the elusive females of a species of Myrmecolacidae (Strepsiptera: Insecta). pp. 117–134. M. Ridley (ed.). Narrow Roads of Gene Land, Vol III. (ed. Mark Ridley). Oxford University Press, Oxford.

    Kathirithamby, J. & Hamilton, W.D. (1992) More covert sex: The elusive females of Myrmecolacidae. Trends in Ecology and Evolution, 7, 349–351.

    Kathirithamby, J. & Johnston, J.S. (2004) The discovery after 94 years of the elusive female of a myrmecolacid (Strepsiptera), and the cryptic species of Caenocholax fenyesi Pierce sensu lato. Proceedings of the Royal Society, Lond. B (Suppl. 3), 271, S5–S8.

    Kjer, K.M. (2004) Aligned 18S and insect phylogeny. Systematic Biology 53, 506-514.

    Kjer, K. M., Blahnik, R. J. & Holzenthal, R. W. (2001) Phylogeny of Trichoptera (Caddisflies): Characterization of signal and noise within multiple datasets. Systematic Biology 50, 781-816.

    Mathews, D.H., Sabina, J., Zuker, M. & Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology, 288, 911–940.

    McCoy, K.D. (2003) What is speciation in parasites- What is sympatry? Trends Parasitology, 19, 400–404.

    de Meeûs, T., Michalakis, Y. & Renaud, F. (1998) Santa Rosalia revisited: ‘or why are there so many kinds of parasites in the garden of earthly delights?’ Parasitology Today, 14, 10–13.

    Schnare, M.N., Damberger, S.M., Gray, M.W. & Gutell, R.R. (1996) Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23S-like) ribosomal RNA. Journal of Molecular Biology, 256, 701–719.

    Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406–3415.