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MBE Advance Access published online on June 27, 2003

Molecular Biology and Evolution, doi:10.1093/molbev/msg167
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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Accepted May 11, 2003
© 2003 Society for Molecular Biology and Evolution

Original Articles

Increased Rates of Sequence Evolution in Endosymbiotic Bacteria and Fungi with Small Effective Population Sizes

Megan Woolfit 1* and Lindell Bromham 1

1 Centre for the Study of Evolution, School of Biological Sciences, University of Sussex, U.K.

* To whom correspondence should be addressed. E-mail: M.R.Q.Woolfit{at}sussex.ac.uk.


   Abstract

Mutualistic, maternally-transmitted endosymbiotic microorganisms undergo severe population bottlenecks at each host generation, resulting in a reduction in effective population size (Ne). Previous studies of Buchnera, the primary endosymbiont of aphids, and several other species of endosymbiotic bacteria, have shown that these species exhibit an increase in the rate of substitution of slightly deleterious mutations, and other predicted effects of increased drift due to small Ne, such as reduced codon bias. However, these studies have been limited in taxonomic scope, and it was therefore not clear whether the increase in rate is a general feature of endosymbiont lineages. Here, we test the prediction that a long-term reduction in Ne causes an increase in substitution rate using DNA sequences of the 16S rRNA gene from thirteen phylogenetically independent comparisons between taxonomically diverse endosymbiotic microorganisms and their free-living relatives. Maximum likelihood and distance-based methods both indicate a significant increase in substitution rate in a wide range of bacterial and fungal endosymbionts compared to closely related free-living lineages. We use this same dataset to test whether 16S genes from endosymbiont display increased A+T content, another indicator of increased genetic drift, and find that there is no significant difference in base composition between endosymbiont and non-endosymbiont 16S genes. However, analysis of an additional dataset of whole bacterial genomes demonstrates that, while host-dependent bacteria have significantly increased genomic A+T content, the base content of the 16S gene tends to vary less than that of the whole genome. It is possible that selection for stability of rRNA is strong enough to overcome the effects of drift towards increased A+T content in endosymbiont 16S genes, despite the reduced effective population sizes of these organisms.

Key Words: symbiosis, yeast-like symbionts, phylogeny, AT bias, relative rate, likelihood ratio test


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