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MBE Advance Access originally published online on January 12, 2008
Molecular Biology and Evolution 2008 25(4):696-708; doi:10.1093/molbev/msn011
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© 2008 The Authors.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Articles

Evidence for Convergent Nucleotide Evolution and High Allelic Turnover Rates at the complementary sex determiner Gene of Western and Asian Honeybees

Martin Hasselmann*, Xavier Vekemans{dagger}, Jochen Pflugfelder{ddagger}, Nikolaus Koeniger{ddagger}, Gudrun Koeniger{ddagger}, Salim Tingek§ and Martin Beye*

* Heinrich-Heine Universitaet Duesseldorf, Institut fuer Genetik, Universitaetsstr, Duesseldorf, Germany
{dagger} Laboratoire de Génétique et Evolution des Populations Végétales, Unité Mixte de Recherche Centre National de Recherche Scientifique 8016, Université de Lille, Villeneuve d'Ascq, France
{ddagger} Institut für Bienenkunde, Johann-Wolfgang-Goethe Universität Frankfurt/M, Oberursel, Germany
§ Agricultural Research Station Tenom, Tenom, Sabah, Malaysia

E-mail: martin.hasselmann{at}uni-duesseldorf.de.

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 these evolutionary forces at the complementary sex determiner (csd) gene that 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 with neutral polymorphisms. Here, we report on the analysis of 17, 19, and 15 csd alleles of Apis cerana, Apis dorsata, and Apis mellifera honeybees, respectively. We observed great heterogeneity of synonymous ({pi}S) and nonsynonymous ({pi}N) polymorphisms across the gene, with a consistent peak in exons 6 and 7. We propose that exons 6 and 7 encode the potential specifying domain (csd-PSD) that 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 ({pi}N/{pi}S ratios are all <1, ranging from 0.6 to 0.95). We observed an excess of shared nonsynonymous changes, which suggest 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 csd-PSD genealogy revealed relatively short average coalescence times (~6 Myr), low average synonymous nucleotide diversity ({pi}S < 0.09), and a lack of trans-specific alleles that 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 turnover 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 historical impact of genetic drift on the molecular evolution of highly social honeybees.

Key Words: sex determination • balancing selection • genetic drift • social insects • convergent adaptive evolution • molecular evolution • nucleotide polymorphism

Diethard Tautz, Associate Editor


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