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Genetics, Vol. 178, 2093-2104, April 2008, Copyright © 2008
doi:10.1534/genetics.107.085787
Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing
Asher D. Cutter*,1,
James D. Wasmuth
and
Nicole L. Washington
* Department of Ecology and Evolutionary Biology and the Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario M5S 3G5, Canada, Program for Molecular Structure and Function, Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada and Life Sciences Division, Lawrence Berkeley National Laboratories, Berkeley, California 94720
1 Corresponding author: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord St., Toronto, ON M5S 3G5, Canada.
E-mail: asher.cutter{at}utoronto.ca
The evolution of self-fertilization can mediate pronounced changes in genomes as a by-product of a drastic reduction in effective population size and the concomitant accumulation of slightly deleterious mutations by genetic drift. In the nematode genus Caenorhabditis, a highly selfing lifestyle has evolved twice independently, thus permitting an opportunity to test for the effects of mode of reproduction on patterns of molecular evolution on a genomic scale. Here we contrast rates of nucleotide substitution and codon usage bias among thousands of orthologous groups of genes in six species of Caenorhabditis, including the classic model organism Caenorhabditis elegans. Despite evidence that weak selection on synonymous codon usage is pervasive in the history of all species in this genus, we find little difference among species in the patterns of codon usage bias and in replacement-site substitution. Applying a model of relaxed selection on codon usage to the C. elegans and C. briggsae lineages suggests that self-fertilization is unlikely to have evolved more than 
4 million years ago, which is less than a quarter of the time since they shared a common ancestor with outcrossing species. We conclude that the profound changes in mating behavior, physiology, and developmental mechanisms that accompanied the transition from an obligately outcrossing to a primarily selfing mode of reproduction evolved in the not-too-distant past.