MBE Advance Access published online on January 12, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn011
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Research Article |
Evidence for convergent nucleotide evolution and high allelic turnover rates at the complementary sex determiner (csd) gene of western and Asian honey bees
* Heinrich-Heine Universitaet Duesseldorf, Institut fuer Genetik, Universitaetsstr. 1, 40225 Duesseldorf, Germany
Laboratoire de Génétique et Evolution des Populations Végétales UMR CNRS 8016, Bâtiment SN2, Université de Lille 1, F-59655 Villeneuve d'Ascq, France
Institut für Bienenkunde, Johann-Wolfgang-Goethe Universität Frankfurt/M, Karl-von-Frisch-Weg 2, 61440 Oberursel, Germany
Agricultural Research Station Tenom, P.O. Box 197, 89908, Tenom, Sabah, Malaysia
to whom correspondence should be addressed: Martin Hasselmann, Martin Beye, Heinrich-Heine Universitaet Duesseldorf, Institut fuer Genetik, Universitaetsstr. 1, 40225 Duesseldorf, Germany, telephone:++49 0211 8114808 ; fax: ++490211 8112279, martin.hasselmann{at}uni-duesseldorf.de, martin.beye{at}uni-duesseldorf.de
Received for publication December 3, 2007. Accepted for publication January 7, 2008.
Our understanding of the impact of recombination, mutation, genetic drift and selection on the evolution of a single gene is still limited. Here we investigate the impact of all of these evolutionary forces at the complementary sex determiner (csd) gene which evolves under a balancing mode of selection. Females are heterozygous at the csd gene and males are hemizygous; diploid males are lethal and occur when csd is homozygous. Rare alleles thus have a selective advantage, are seldom lost by the effect of genetic drift and are maintained over extended periods of time when compared to neutral polymorphisms. Here, we report on the analysis of 17, 19 and 15 csd alleles of Apis cerana, Apis dorsata and Apis mellifera honey bees respectively. We observed great heterogeneity of synonymous (
S) and nonsynonymous (N) polymorphisms across the gene, with a consistent peak in exon 6 and 7. We propose that exons 6 and 7 encode the potential specifying domain (csd-PSD) which has accumulated elevated nucleotide polymorphisms over time by balancing selection. We observed no direct evidence that balancing selection favors the accumulation of nonsynonymous changes at csd-PSD (N/S ratios are all < 1, ranging from 0.6 to 0.95). We observed an excess of shared nonsynonymous changes, which suggests that strong evolutionary constraints are operating at csd-PSD resulting in the independent accumulation of the same nonsynonymous changes in different alleles across species (convergent evolution). Analysis of a csd-PSD genealogy revealed relatively short average coalescence times (
6 million years), low average synonymous nucleotide diversity (S < 0.09) and a lack of trans-specific alleles which substantially contrasts with previously analyzed loci under strong balancing selection. We excluded the possibility of a burst of diversification after population bottlenecking and intragenic recombination as explanatory factors, leaving high turn-over rates as the explanation for this observation. By comparing observed allele richness and average coalescence times with a simplified model of csd-coalescence, we found that small long term population sizes (i.e. Ne <104), but not high mutation rates, can explain short maintenance times, implicating a strong impact of genetic drift on the molecular evolution of highly social honey bees.
Key Words: sex determination • balancing selection • genetic drift • social insects • convergent adaptive evolution • molecular evolution • nucleotide polymorphism