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MBE Advance Access published online on December 15, 2005

Molecular Biology and Evolution, doi:10.1093/molbev/msj074
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted December 12, 2005

Research Article

Rapid Evolution and Gene-specific Patterns of Selection for Three Genes of Spermatogenesis in Drosophila

Alberto Civetta 1 *, Sujeetha A. Rajakumar 2, Barb Brouwers 1, and John P. Bacik 3

1 Department of Biology, University of Winnipeg
2 Department of Biology, University of Winnipeg; Department of Biochemistry and Medical Genetics, University of Manitoba; Current address: Lady Davis Institute for Medical Research, McGill University, Montreal, QC
3 Department of Biology, University of Winnipeg; Current address: Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB

* To whom correspondence should be addressed.
Alberto Civetta, E-mail: a.civetta{at}uwinnipeg.ca


   Abstract

Hybrid males resulting from crosses between closely related species of Drosophila are sterile. The F1 hybrid sterility phenotype is mainly due to defects occurring during late stages of development that relate to sperm individualization, and so genes controlling sperm development may have been subjected to selective diversification between species. It is also possible that genes of spermatogenesis experience selective constraints given their role in a developmental pathway. We analyzed the molecular evolution of three genes playing a role during the sperm developmental pathway in Drosophila at an early (bam), a mid (aly) and a late (dj) stage. The complete coding region of these genes was sequenced in different strains of Drosophila melanogaster and D. simulans. All three genes showed rapid divergence between species, with larger numbers of nonsynonymous to synonymous differences between species than polymorphisms. Although this could be interpreted as evidence for positive selection at all three genes, formal tests of selection do not support such conclusion. Departures from neutrality were detected only for dj and bam but not aly. The role played by selection is unique and determined by gene-specific characteristics rather than site of expression. In dj, the departure was due to a high proportion of neutral synonymous polymorphisms in D. simulans and there was evidence of purifying selection maintaining a high lysine amino acid protein content that is characteristic of other DNA binding proteins. The earliest spermatogenesis gene surveyed, which plays a role in both male and female gametogenesis, was bam and its significant departure from neutrality was due to an excess of nonsynonymous substitutions between species. Bam is degraded at the end of mitosis and rapid evolutionary changes among species might be a characteristic shared with other degradable transient proteins. However, the large number of nonsynonymous changes between D. melanogaster and D. simulans and a phylogenetic comparative analysis among species confirms evidence of positive selection driving the evolution of Bam and suggests an yet unknown germ-cell line developmental adaptive change between these two species.

Keywords: population genetics; spermatogenesis; Drosophila; selection.
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