Journal of Molecular Evolution

, Volume 41, Issue 6, pp 727–731 | Cite as

Faster evolutionary rates in endosymbiotic bacteria than in cospeciating insect hosts

  • Nancy A. Moran
  • Carol D. von Dohlen
  • Paul Baumann
Articles

Abstract

The hypothesis of a universal molecular clock holds that divergent lineages exhibit approximately constant rates of nucleotide substitution over evolutionary time for a particular macromolecule. We compare divergences of ribosomal DNA for aphids (Insecta) and Buchnera, the maternally transmitted, endosymbiotic bacteria that have cospeciated with aphids since initially infecting them over 100 million years ago. Substitution rates average 36 times greater for Buchnera than for their aphid hosts for regions of small-subunit rDNA that are homologous for prokaryotes and eukaryotes. Aphids exhibit 18S rDNA substitution rates that are within the range observed in related insects. In contrast, 16S rDNA evolves about twice as fast in Buchnera as in related free-living bacterial lineages. Nonetheless, the difference between Buchnera and aphids is much greater, suggesting that rates may be generally higher in bacteria. This finding adds to evidence that molecular clocks are only locally rather than universally valid among taxonomic groups. It is consistent with the hypothesis that rates of sequence evolution depend on generation time.

Key words

Aphid Bacteria Buchnera Cospeciation Endosymbiosis Evolutionary rates Molecular clock Prokaryote Ribosomal DNA 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baumann P, Baumann L, Lai C-Y, Rouhbakhsh D, Moran NA, Clark MA (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:51–94Google Scholar
  2. Bousquet J, Strauss SH, Doerksen AH, Price RA (1992) Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc Natl Acad Sci USA 89:7844–7848Google Scholar
  3. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New YorkGoogle Scholar
  4. Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971Google Scholar
  5. Dickerson RE (1971) The structure of cytochrome c and the rate of molecular evolution. J Mol Evol 1:26–45Google Scholar
  6. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434Google Scholar
  7. Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Philol Trans R Soc Lond [Biol] 312:275–289Google Scholar
  8. Gaut BS, Muse SV, Clark WD, Clegg MT (1992) Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants. J Mol Evol 35:292–303Google Scholar
  9. Gutell RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–216Google Scholar
  10. Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Nadler SA (1994) Disparate rates of molecular evolution in cospeciating hosts and parasites Science 265:1087–1090Google Scholar
  11. Harvey PH, May RM (1993) Bacterial tick-tock. Nature 365:492Google Scholar
  12. Heie OE (1987) Paleontology and phylogeny. In: Minks AK, Harrewijn P (eds) Aphids, their biology, natural enemies, and control. World crop pests Vol 2A. Elsevier, Amsterdam, pp 367–391Google Scholar
  13. Hendriks L, van Broekhoven C, Vandenberghe A, Van de Peer, Y, de Wachter R (1988) Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma califomica and evolutionary relationships among eukaryotic phyla. Eur J Biochem 177:15–20Google Scholar
  14. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132Google Scholar
  15. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, New YorkGoogle Scholar
  16. Kwon O-Y, Ogino K, Ishikawa H (1991) The longest 18S ribosomal RNA ever known: nucleotide sequence and presumed secondary structure of the 18S rRNA of the pea aphid, Acyrthosiphon pisum. Eur J Biochem 202:827–833Google Scholar
  17. Lai C-Y, Baumann P (1992) Genetic analysis of an aphid endosymbiont DNA fragment homologous to the rnpa-trpmH-dnaA-dnaN-gyrB region of eubacteria. Gene 113:175–181Google Scholar
  18. Li W-H (1993) What about the molecular clock hypothesis? Curr Opin Genet Dev 3:896–901Google Scholar
  19. Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342Google Scholar
  20. Martin AP, Palumbi SR (1993) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Proc Natl Acad Sci USA 90:4087–4091Google Scholar
  21. Moran NA (1989) A 48-million-year-old aphid-host plant association and complex life cycle: biogeographic evidence. Science 245:173–175Google Scholar
  22. Moran NA, Baumann P (1994) Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Tr Ecol Evol 9:15–20Google Scholar
  23. Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond [Biol] 253:167–171Google Scholar
  24. Munson MA, Baumann L, Baumann P (1993) Buchnera aphidicola (a prokaryotic endosymbiont of aphids) contain a putative 16S rRNA operon unlinked to the 23S rRNA-encoding gene: sequence determination, and promoter and terminator analysis. Gene 137:171–178Google Scholar
  25. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, Campbell BC (1991a) Aphid-eubacterial endosymbiosis: evidence for its establishment in an ancestor of four aphid families. J Bacteriol 173:6321–6324Google Scholar
  26. Munson MA, Baumann P, Kinsey MG (1991b) Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyteassociated, primary endosymbionts of aphids. Int J Syst Bacteriol 41:566–568Google Scholar
  27. Nickrent DL, Starr EM (1994) High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparastic flowering plants. J Mol Evol 39:62–70Google Scholar
  28. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86Google Scholar
  29. Vawter L Brown WN (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196Google Scholar
  30. Voegtlin D (1995) Notes on the Mindarus species (Homoptera: Aphididae) of North America with descriptions of two new species. Proc Entomol Soc Wash 97:178–196Google Scholar
  31. von Dohlen CD, Moran NA (1995) Molecular phylogeny of the Homoptera: a paraphyletic taxon. J Mol Evol 41:211–223Google Scholar
  32. Woese CR (1987) Bacterial evolution. Microbiol Rev 52:221–271Google Scholar
  33. Wolfe KH, LI W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058Google Scholar
  34. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8:357–366PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1995

Authors and Affiliations

  • Nancy A. Moran
    • 1
  • Carol D. von Dohlen
    • 1
  • Paul Baumann
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Microbiology SectionUniversity of California-DavisDavisUSA

Personalised recommendations