Journal of Molecular Evolution

, Volume 59, Issue 6, pp 849–858 | Cite as

Mutation Exposed: A Neutral Explanation for Extreme Base Composition of an Endosymbiont Genome

Article

Abstract

The influence of neutral mutation pressure versus selection on base composition evolution is a subject of considerable controversy. Yet the present study represents the first explicit population genetic analysis of this issue in prokaryotes, the group in which base composition variation is most dramatic. Here, we explore the impact of mutation and selection on the dynamics of synonymous changes in Buchnera aphidicola, the AT-rich bacterial endosymbiont of aphids. Specifically, we evaluated three forms of evidence. (i) We compared the frequencies of directional base changes (AT→GC vs. GC→AT) at synonymous sites within and between Buchnera species, to test for selective preference versus effective neutrality of these mutational categories. Reconstructed mutational changes across a robust intraspecific phylogeny showed a nearly 1:1 AT→GC:GC→AT ratio. Likewise, stationarity of base composition among Buchnera species indicated equal rates of AT→GC and GC→AT substitutions. The similarity of these patterns within and between species supported the neutral model. (ii) We observed an equivalence of relative per-site AT mutation rate and current AT content at synonymous sites, indicating that base composition is at mutational equilibrium. (iii) We demonstrated statistically greater equality in the frequency of mutational categories in Buchnera than in parallel mammalian studies that documented selection on synonymous sites. Our results indicate that effectively neutral mutational pressure, rather than selection, represents the major force driving base composition evolution in Buchnera. Thus they further corroborate recent evidence for the critical role of reduced N e in the molecular evolution of bacterial endosymbionts.

Keywords

Mutation Selection Base composition Drift DNA repair Buchnera Neutrality 

Notes

Acknowledgments

The authors thank Jonas Sandström and Nancy Moran for collecting the Uroleucon samples used in the interspecific analysis, and Paul Baumann for DNA extractions of several of these isolates. We are grateful to Steve Pennings for providing the Georgia isolate of U. ambrosiae, thank David McCauley for discussion of statistical issues, and are indebted to two anonymous reviewers for helpful comments on an earlier version of this paper. We appreciate the helpful advice and correspondence of Nancy Moran, Nicolas Galtier, Hiroshi Akashi, and Adam Eyre-Walker during the analyses for this study. We thank Patrick Degnan for superb technical assistance. The present study was conducted with support provided by the NIH (R01 GM62626-01), NSF (DEB 0089455), NASA Astrobiology Institute (NNA04CC04A), and Josephine Bay Paul and C. Michael Paul Foundation to J.J.W. Support to D.J.F. was provided by Vanderbilt University. DNA sequencing was performed at the Josephine Bay Paul Center’s W.M. Keck Ecological and Evolutionary Genetics Facility.

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Copyright information

© Springer Science + Business Media Inc. 2004

Authors and Affiliations

  1. 1.Josephine Bay Paul Center for Comparative Molecular Biology & EvolutionThe Marine Biological LaboratoryWoods HoleUSA
  2. 2.Department of Biological SciencesVanderbilt UniversityNashvilleUSA

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