Skip to main content
SpringerLink
Log in

Molecular Evidence for Polyphyletic Origin of the Primary Symbionts of Sucking Lice (Phthiraptera, Anoplura)

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Based on 16S rDNA analyses, the primary symbionts of sucking lice were found to form a polyphyletic assemblage of several distant lineages that have arisen several times within Enterobacteriaceae and at least once within Legionellaceae. Another independent lineage of endosymbiotic enterobacteria inhabits a sister group of the sucking lice, Rhynchophthirina. The inspection of 16S rDNA supports the symbiotic nature of the investigated bacteria; they display a typical trait of degenerative processes, an increased AT content (Adenine–Thymine content) in comparison with free-living bacteria. The calculation of divergence time between the closest anopluran and rhynchophthirine symbionts further support their independent origin. The results shown here, together with evidence from other groups, indicate that the significance of primary symbionts for blood-feeding insects should be reconsidered.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Aksoy, S, Pourhosseini, AA, Chow, A (1995) Mycetome endosymbionts of tsetse flies constitute a distinct lineage related to Enterobacteriaceae. Insect Mol Biol 4: 5–22

    Google Scholar 

  2. Aschner, M (1934) Studies on the symbiosis of body louse. Elimination of the symbionts by centrifugation of the eggs. Parasitology 26: 309–314

    Google Scholar 

  3. Bandi, C, Sironi, M, Damiani, G, Magrassi, L, Nalepa, CA, Laudani, U, Sacchi, L (1995) The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond B 259: 293–299

    Article  CAS  Google Scholar 

  4. Barker, SC, Whiting, M, Johnson, KP, Murrell, A (2002) Phylogeny of the lice (Insecta, Phthiraptera) inferred from small subunit rRNA. Zool Scr 32: 407–414

    Article  Google Scholar 

  5. Baumann, P, Moran, NA, Baumann, L (1997) The evolution and genetics of aphid symbionts. Bioscience 47: 12–20

    Article  Google Scholar 

  6. Baumann, P, Moran, NA (1997) Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie van Leeuwenhoek 72: 39–48

    Article  PubMed  CAS  Google Scholar 

  7. Baumann, P, Moran, NA, Baumann, L (2000) Bacteriocyte-associated endosymbionts in insect. Curr Opin Microbiol 3: 270–275

    Article  PubMed  Google Scholar 

  8. Bender, W, Spierer, P, Hogness, DS (1983) Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol 168: 17–33

    Article  PubMed  CAS  Google Scholar 

  9. Brynnel, UE, Kurland, CG, Moran, NA, Andersson, SGE (1998) Evolutionary rates for tuf genes in endosymbionts of aphids. Mol Biol Evol 15: 574–582

    PubMed  CAS  Google Scholar 

  10. Buchner P (1965) Endosymbiosis of Animals with Plant Microorganisms. John Wiley and Sons, New York

    Google Scholar 

  11. Clark, M, Moran, NA, Baumann, P, Wernergreen, JJ (2000) Cospeciation between bacterial endosymbionts (Buchnera) and recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54: 517–525

    PubMed  CAS  Google Scholar 

  12. Chen, X, Li, S, Aksoy, S, (1999) Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48: 49–58

    Article  PubMed  CAS  Google Scholar 

  13. Douglas, AE, (1989) Mycetocyte symbionts in insects. Biol Rev 64: 409–434

    PubMed  CAS  Google Scholar 

  14. Eberle, MW, McLean, DL, (1983) Observation of symbiote migration in human body lice with scanning and transmission electron microscopy. Can J Microbiol 28: 755–762

    Article  Google Scholar 

  15. Frank, SA, (1996) Host control of symbiont transmission: the separation of symbionts into germ and soma. Am Nat 148: 1113–1124

    Article  Google Scholar 

  16. Fukatsu, T (2001) Secondary intracellular symbiotic bacteria in aphids of the Genus Yamatocallis (Homoptera: Aphididae: Drepanosiphinae). Appl Environ Microbiol 67: 5315–5320

    Article  PubMed  CAS  Google Scholar 

  17. Griffiths, GW, Beck, SD (1974) Effects of antibiotics on intracellular symbionts in pea Aphids, Acyrtosiphon pisum. Cell Tissue Res 148: 287–300

    Article  PubMed  CAS  Google Scholar 

  18. Guindon, S, Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704

    Article  PubMed  Google Scholar 

  19. Hill, PDS, Campbell, JA (1973) The production of symbiont-free Glossina morsitans and an associated loss of female fertility. Trans R Soc Trop Med Hyg 67: 727–728

    Article  PubMed  CAS  Google Scholar 

  20. Huelsenbeck, JP, Ronquist, F (2001) Mr.Bayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

    Article  PubMed  CAS  Google Scholar 

  21. Itoh, T, Martin, W, Nei, M (2002) Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA 99: 12944–12948

    Article  PubMed  CAS  Google Scholar 

  22. Johnson, KP, Whiting, MF (2001) Multiple genes and the monophyly of Ischnocera (Insecta: Phthiraptera). Mol Phylogenet Evol 22: 101–110

    Article  CAS  Google Scholar 

  23. Johnson, KP, Yoshizawa, K, Smith, VS (2004) Multiple origin of parasitism in lice. Proc R Soc Lond B 271: 1771–1776

    Article  Google Scholar 

  24. Kyei-Poku, GK, Colwell, DD, Coghlin, P, Benkel B, Floate, KD (2005) On the ubiquity and phylogeny of Wolbachia in lice. Mol Ecol 14: 285–294

    Article  PubMed  CAS  Google Scholar 

  25. Kim KC (1985) Coevolution of Parasitic Arthropods and Mammals. John Wiley, New York

    Google Scholar 

  26. Kumar, S, Tamura, K, Jakobsen, IB, Nei, M (2001) MEGA2, Molecular evolutionary genetics analysis software. Bioinformatics 17: 1244–1245

    Article  PubMed  CAS  Google Scholar 

  27. Lambert, DJ, Moran, NA (1998) Deleterious mutations destabilize ribosomal DNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95: 4458–4462

    Article  PubMed  CAS  Google Scholar 

  28. Li, WH (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36: 96–99

    Article  PubMed  CAS  Google Scholar 

  29. Mira, A, Moran, NA (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microbiol Ecol 44: 137–143

    Article  CAS  Google Scholar 

  30. Moran, N, Telang, A (1998) Bacteriocyte-associated symbionts of insects. BioScience 48: 295–304

    Article  Google Scholar 

  31. Moran, NA (1996) Accelerated evolution and Müller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93: 2873–2878

    Article  PubMed  CAS  Google Scholar 

  32. Munson, MA, Baumann, P, Clark, MA, Baumann, L, Moran, NA, Voegtlin, DJ (1991) Evidence for the establishment of aphid–eubacterial endosymbiosis in an ancestor of four aphid families. J Bacteriol 173: 6321–6324

    PubMed  CAS  Google Scholar 

  33. Munson, MA, Baumann, P, Moran, NA (1992) Phylogenetic relationships of the endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Mol Phylogenet Evol 1: 26–30

    Article  PubMed  CAS  Google Scholar 

  34. Nogge, G (1976) Sterility of tsetse flies caused by loss of symbionts. Experentia 32: 995

    Article  CAS  Google Scholar 

  35. Nogge, G (1978) Aposymbiotic tsetse flies, Glossna morsitans morsitans, obtained by feeding on rabbits immunized specifically with symbionts. J Insect Physiol 24: 299–304

    Article  PubMed  CAS  Google Scholar 

  36. O’Neil, S, Giordano, R, Colbert, AME, Karr, TL, Robertson, HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89: 2699–2702

    Article  Google Scholar 

  37. O’Neill, S, Gooding, RH, Aksoy, S (1993) Phylogenetically distant symbiotic organisms reside in Glossina midgut and ovary tissues. Med Vet Entomol 7: 377–383

    PubMed  CAS  Google Scholar 

  38. Perotti, MA, Catalá, SS, Ormeño, AV, Żelazowska, M, Biliński, SM, Braig, HR (2004) The sex ratio distortion in the human head louse is conserved over time. BMC Genetics 5: 10

    Article  PubMed  Google Scholar 

  39. Posada, D, Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818

    Article  PubMed  CAS  Google Scholar 

  40. Puchta, O (1955) Experimentelle Untersuchungen űber die Bedeutung der symbiose der Kleiderlaus Pediculus vestimenti Burm. Z Parastenkd 17: 1–40

    CAS  Google Scholar 

  41. Reed, DL, Hafner, MS (2002) Phylogenetic analysis of bacterial communities associated with ectoparasitic chewing lice of pocket gophers: a culture independent approach. Microbiol Ecol 44: 48–93

    Article  CAS  Google Scholar 

  42. Ries, E (1931) Die Symbiose der Läuse und Federlinge. Z Morphol Ökol Tiere 20: 233–367

    Article  Google Scholar 

  43. Sandström, JP, Russel, JA, White, JP, Moran, NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10: 217–228

    Article  PubMed  Google Scholar 

  44. Sasaki-Fukatsu, K, Koga, R, Nikoh, N, Yoshizawa, K, Kasai, S, Mihara, M, Kobayashi, M, Tomita, T, Fukatsu, T (2006) Symbiotic bacteria associated with stomach discs of human lice. Appl Environ Microbiol 72: 7349–7352

    Article  PubMed  CAS  Google Scholar 

  45. Schröder, D, Deppisch, H, Obermeyer, M, Krone, G, Stackebrandt, E, Holldobler, B, Goebel, W, Gross, R (1996) Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol Microbiol 21: 479–489

    Article  PubMed  Google Scholar 

  46. Spaulding, AW, von Dohlen, CD (2001) Psyllids endosymbionts exhibit patterns of co-speciation with hosts and destabilizing substitutions in ribosomal RNA. Insect Mol Biol 10: 57–67

    Article  PubMed  CAS  Google Scholar 

  47. Syvänen, AC, Amiri, H, Jamal, A, Andersson, SGE, Kurland, GC (1996) A chimeric disposition of the elongation factor genes in Rickettsia prowazeki. J Bacteriol 178: 6192–6199

    PubMed  Google Scholar 

  48. Swofford, DL (1998) PAUP 4.0—phylogenetic analysis using parsimony. Version 4. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  49. Thao, ML, Moran, NA, Abbot, P, Brennan, EB, Burckhardt, DH, Baumann, P (2000) Cospeciation of psyllids and their primary procaryotic endosymbionts. Appl Environ Microbiol 66: 2898–2905

    Article  PubMed  CAS  Google Scholar 

  50. Thompson, JD, Higgins, DG, Gibson, TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680

    Article  PubMed  CAS  Google Scholar 

  51. Volf, P (1991) Postembryonal development of Mycetocytes and symbionts of the spiny rat louse Polyplax spinulosa. J Invertebr Pathol 58: 143–146

    Article  Google Scholar 

  52. Wernegreen, JJ, Moran, NA (1999) Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol 16: 83–97

    PubMed  CAS  Google Scholar 

  53. Wernergreen, JJ, Funk, DJ (2004) Mutation exposed: a natural explanation for extreme base composition of endosymbiont genome. J Mol Evol 59: 849–858

    Article  CAS  Google Scholar 

  54. Żelazowska, M, Biliński, SM (1999) Distribution and transmission of endosymbiotic mocroorgnisms in the oocytes of the pig louse, Haematopinus suis (L.) (Insecta: Phthiraptera). Protoplasma 209: 207–213

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Břetislav Koudela, Kathy Stafford, and Ján Krištofík for providing the lice samples, and to anonymous reviewers for important comments. This work was supported by Grants 206/04/0520 (Grant Agency of the Czech Republic) and MSM 60076605801 (Ministry of Education, Czech Republic).

Author information

Authors and Affiliations

  1. Faculty of Biological Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Václav Hypša & Jaroslav Křížek

  2. Institute of Parasitology AS CR, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Václav Hypša

Authors
  1. Václav Hypša
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaroslav Křížek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Václav Hypša.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hypša, V., Křížek, J. Molecular Evidence for Polyphyletic Origin of the Primary Symbionts of Sucking Lice (Phthiraptera, Anoplura). Microb Ecol 54, 242–251 (2007). https://doi.org/10.1007/s00248-006-9194-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9194-x

Keywords

Search

Navigation