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Two Rapidly Evolving Genes Contribute to Male Fitness in Drosophila

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Abstract

Purifying selection often results in conservation of gene sequence and function. The most functionally conserved genes are also thought to be among the most biologically essential. These observations have led to the use of sequence conservation as a proxy for functional conservation. Here we describe two genes that are exceptions to this pattern. We show that lack of sequence conservation among orthologs of CG15460 and CG15323—herein named jean-baptiste (jb) and karr, respectively—does not necessarily predict lack of functional conservation. These two Drosophila melanogaster genes are among the most rapidly evolving protein-coding genes in this species, being nearly as diverged from their D. yakuba orthologs as random sequences are. jb and karr are both expressed at an elevated level in larval males and adult testes, but they are not accessory gland proteins and their loss does not affect male fertility. Instead, knockdown of these genes in D. melanogaster via RNA interference caused male-biased viability defects. These viability effects occur prior to the third instar for jb and during late pupation for karr. We show that putative orthologs to jb and karr are also expressed strongly in the testes of other Drosophila species and have similar gene structure across species despite low levels of sequence conservation. While standard molecular evolution tests could not reject neutrality, other data hint at a role for natural selection. Together these data provide a clear case where a lack of sequence conservation does not imply a lack of conservation of expression or function.

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Acknowledgments

The authors wish to thank Manyuan Long and three anonymous reviewers for comments and suggestions on the manuscript and study design. We thank Sidi Chen and Nicholas VanKuren from Manyuan Long’s lab for the Actin-GAL4; UAS-GFP stock, and Helen White-Cooper for the tombola null stock. We thank Teni Coker, Betty Wanjiru, Anais Monroy, Alicia Brandt, and Sophia Shih for technical assistance. This work was supported by NSF grant MCB 0920196 to CDJ and a Royster Society Fellowship to JAR.

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Correspondence to Josephine A. Reinhardt.

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Reinhardt, J.A., Jones, C.D. Two Rapidly Evolving Genes Contribute to Male Fitness in Drosophila . J Mol Evol 77, 246–259 (2013). https://doi.org/10.1007/s00239-013-9594-8

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  • DOI: https://doi.org/10.1007/s00239-013-9594-8

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