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. 2001 Feb;157(2):477–489. doi: 10.1093/genetics/157.2.477

Intraspecific variation in symbiont genomes: bottlenecks and the aphid-buchnera association.

D J Funk 1, J J Wernegreen 1, N A Moran 1
PMCID: PMC1461510  PMID: 11156972

Abstract

Buchnera are maternally transmitted bacterial endosymbionts that synthesize amino acids that are limiting in the diet of their aphid hosts. Previous studies demonstrated accelerated sequence evolution in Buchnera compared to free-living bacteria, especially for nonsynonymous substitutions. Two mechanisms may explain this acceleration: relaxed purifying selection and increased fixation of slightly deleterious alleles under drift. Here, we test the divergent predictions of these hypotheses for intraspecific polymorphism using Buchnera associated with natural populations of the ragweed aphid, Uroleucon ambrosiae. Contrary to expectations under relaxed selection, U. ambrosiae from across the United States yielded strikingly low sequence diversity at three Buchnera loci (dnaN, trpBC, trpEG), revealing polymorphism three orders of magnitude lower than in enteric bacteria. An excess of nonsynonymous polymorphism and of rare alleles was also observed. Local sampling of additional dnaN sequences revealed similar patterns of polymorphism and no evidence of food plant-associated genetic structure. Aphid mitochondrial sequences further suggested that host bottlenecks and large-scale dispersal may contribute to genetic homogenization of aphids and symbionts. Together, our results support reduced N(e) as a primary cause of accelerated sequence evolution in Buchnera. However, our study cannot rule out the possibility that mechanisms other than bottlenecks also contribute to reduced N(e) at aphid and endosymbiont loci.

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Selected References

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  1. ATWOOD K. C., SCHNEIDER L. K., RYAN F. J. Selective mechanisms in bacteria. Cold Spring Harb Symp Quant Biol. 1951;16:345–355. doi: 10.1101/sqb.1951.016.01.026. [DOI] [PubMed] [Google Scholar]
  2. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14043–14048. doi: 10.1073/pnas.96.24.14043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akashi H. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics. 1996 Nov;144(3):1297–1307. doi: 10.1093/genetics/144.3.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baumann L., Baumann P., Moran N. A., Sandström J., Thao M. L. Genetic characterization of plasmids containing genes encoding enzymes of leucine biosynthesis in endosymbionts (Buchnera) of aphids. J Mol Evol. 1999 Jan;48(1):77–85. doi: 10.1007/pl00006447. [DOI] [PubMed] [Google Scholar]
  5. Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
  6. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [DOI] [PubMed] [Google Scholar]
  7. Bergstrom C. T., Pritchard J. Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics. 1998 Aug;149(4):2135–2146. doi: 10.1093/genetics/149.4.2135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bracho A. M., Martínez-Torres D., Moya A., Latorre A. Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi. J Mol Evol. 1995 Jul;41(1):67–73. doi: 10.1007/BF00174042. [DOI] [PubMed] [Google Scholar]
  9. Brynnel E. U., Kurland C. G., Moran N. A., Andersson S. G. Evolutionary rates for tuf genes in endosymbionts of aphids. Mol Biol Evol. 1998 May;15(5):574–582. doi: 10.1093/oxfordjournals.molbev.a025958. [DOI] [PubMed] [Google Scholar]
  10. Charles H., Ishikawa H. Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. J Mol Evol. 1999 Feb;48(2):142–150. doi: 10.1007/pl00006452. [DOI] [PubMed] [Google Scholar]
  11. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clark M. A., Moran N. A., Baumann P. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol. 1999 Nov;16(11):1586–1598. doi: 10.1093/oxfordjournals.molbev.a026071. [DOI] [PubMed] [Google Scholar]
  13. Clark M. A., Moran N. A., Baumann P., Wernegreen J. J. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution. 2000 Apr;54(2):517–525. doi: 10.1111/j.0014-3820.2000.tb00054.x. [DOI] [PubMed] [Google Scholar]
  14. De Barro P. J., Sherratt T. N., Carvalho G. R., Nicol D., Iyengar A., MacLean N. Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe. Mol Ecol. 1995 Jun;4(3):375–382. doi: 10.1111/j.1365-294x.1995.tb00230.x. [DOI] [PubMed] [Google Scholar]
  15. Douglas A. E. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998;43:17–37. doi: 10.1146/annurev.ento.43.1.17. [DOI] [PubMed] [Google Scholar]
  16. Ehrlich P. R., Raven P. H. Differentiation of populations. Science. 1969 Sep 19;165(3899):1228–1232. doi: 10.1126/science.165.3899.1228. [DOI] [PubMed] [Google Scholar]
  17. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fu Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997 Oct;147(2):915–925. doi: 10.1093/genetics/147.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Funk D. J., Helbling L., Wernegreen J. J., Moran N. A. Intraspecific phylogenetic congruence among multiple symbiont genomes. Proc Biol Sci. 2000 Dec 22;267(1461):2517–2521. doi: 10.1098/rspb.2000.1314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hasegawa M., Cao Y., Yang Z. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol Biol Evol. 1998 Nov;15(11):1499–1505. doi: 10.1093/oxfordjournals.molbev.a025877. [DOI] [PubMed] [Google Scholar]
  21. Lai C. Y., Baumann L., Baumann P. Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3819–3823. doi: 10.1073/pnas.91.9.3819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lynch M. Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes. Mol Biol Evol. 1997 Sep;14(9):914–925. doi: 10.1093/oxfordjournals.molbev.a025834. [DOI] [PubMed] [Google Scholar]
  23. Lynch M. Mutation accumulation in transfer RNAs: molecular evidence for Muller's ratchet in mitochondrial genomes. Mol Biol Evol. 1996 Jan;13(1):209–220. doi: 10.1093/oxfordjournals.molbev.a025557. [DOI] [PubMed] [Google Scholar]
  24. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  25. Moran N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873–2878. doi: 10.1073/pnas.93.7.2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Munson M. A., Baumann P., Clark M. A., Baumann L., Moran N. A., Voegtlin D. J., Campbell B. C. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991 Oct;173(20):6321–6324. doi: 10.1128/jb.173.20.6321-6324.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nei M., Li W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5269–5273. doi: 10.1073/pnas.76.10.5269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ochman H., Elwyn S., Moran N. A. Calibrating bacterial evolution. Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12638–12643. doi: 10.1073/pnas.96.22.12638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohta T. Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. J Mol Evol. 1995 Jan;40(1):56–63. doi: 10.1007/BF00166595. [DOI] [PubMed] [Google Scholar]
  30. Peek A. S., Vrijenhoek R. C., Gaut B. S. Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol. 1998 Nov;15(11):1514–1523. doi: 10.1093/oxfordjournals.molbev.a025879. [DOI] [PubMed] [Google Scholar]
  31. Rand D. M., Kann L. M. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 1996 Jul;13(6):735–748. doi: 10.1093/oxfordjournals.molbev.a025634. [DOI] [PubMed] [Google Scholar]
  32. Rand D. M., Kann L. M. Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica. 1998;102-103(1-6):393–407. [PubMed] [Google Scholar]
  33. Rouhbakhsh D., Clark M. A., Baumann L., Moran N. A., Baumann P. Evolution of the tryptophan biosynthetic pathway in Buchnera (aphid endosymbionts): studies of plasmid-associated trpEG within the genus Uroleucon. Mol Phylogenet Evol. 1997 Oct;8(2):167–176. doi: 10.1006/mpev.1997.0419. [DOI] [PubMed] [Google Scholar]
  34. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  35. Simon J. C., Baumann S., Sunnucks P., Hebert P. D., Pierre J. S., Le Gallic J. F., Dedryver C. A. Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Mol Ecol. 1999 Apr;8(4):531–545. doi: 10.1046/j.1365-294x.1999.00583.x. [DOI] [PubMed] [Google Scholar]
  36. Simon J. C., Martinez-Torres D., Latorre A., Moya A., Hebert P. D. Molecular characterization of cyclic and obligate parthenogens in the aphid Rhopalosiphum padi (L.). Proc Biol Sci. 1996 Apr 22;263(1369):481–486. doi: 10.1098/rspb.1996.0072. [DOI] [PubMed] [Google Scholar]
  37. Spaulding A. W., von Dohlen C. D. Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (Hemiptera: Sternorrhyncha). Mol Biol Evol. 1998 Nov;15(11):1506–1513. doi: 10.1093/oxfordjournals.molbev.a025878. [DOI] [PubMed] [Google Scholar]
  38. Sreevatsan S., Pan X., Stockbauer K. E., Connell N. D., Kreiswirth B. N., Whittam T. S., Musser J. M. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9869–9874. doi: 10.1073/pnas.94.18.9869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sunnucks P., De Barro P. J., Lushai G., Maclean N., Hales D. Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Mol Ecol. 1997 Nov;6(11):1059–1073. doi: 10.1046/j.1365-294x.1997.00280.x. [DOI] [PubMed] [Google Scholar]
  40. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
  41. Wernegreen J. J., Moran N. A. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol. 1999 Jan;16(1):83–97. doi: 10.1093/oxfordjournals.molbev.a026040. [DOI] [PubMed] [Google Scholar]
  42. Wilson AC, Sunnucks P, Hales DF. Microevolution, low clonal diversity and genetic affinities of parthenogenetic sitobion aphids in new zealand. Mol Ecol. 1999 Oct;8(10):1655–1666. doi: 10.1046/j.1365-294x.1999.00751.x. [DOI] [PubMed] [Google Scholar]
  43. van Ham R. C., Moya A., Latorre A. Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids). J Bacteriol. 1997 Aug;179(15):4768–4777. doi: 10.1128/jb.179.15.4768-4777.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]

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