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Open Access Research article

Demasculinization of the Anopheles gambiae X chromosome

Kalle Magnusson1, Gareth J Lycett2, Antonio M Mendes1, Amy Lynd2, Philippos-Aris Papathanos13, Andrea Crisanti1 and Nikolai Windbichler1*

Author affiliations

1 Imperial College London, Department of Life Sciences, Imperial College Road, London, SW7 2AZ, UK

2 Liverpool School of Tropical Medicine, Pembroke Place, London, L3 5QA, UK

3 Division of Biology; California Institute of Technology, Pasadena, CA, USA

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Citation and License

BMC Evolutionary Biology 2012, 12:69  doi:10.1186/1471-2148-12-69

Published: 18 May 2012

Abstract

Background

In a number of organisms sex-biased genes are non-randomly distributed between autosomes and the shared sex chromosome X (or Z). Studies on Anopheles gambiae have produced conflicting results regarding the underrepresentation of male-biased genes on the X chromosome and it is unclear to what extent sexual antagonism, dosage compensation or X-inactivation in the male germline, the evolutionary forces that have been suggested to affect the chromosomal distribution of sex-biased genes, are operational in Anopheles.

Results

We performed a meta-analysis of sex-biased gene expression in Anopheles gambiae which provides evidence for a general underrepresentation of male-biased genes on the X-chromosome that increased in significance with the observed degree of sex-bias. A phylogenomic comparison between Drosophila melanogaster, Aedes aegypti and Culex quinquefasciatus also indicates that the Anopheles X chromosome strongly disfavours the evolutionary conservation of male-biased expression and that novel male-biased genes are more likely to arise on autosomes. Finally, we demonstrate experimentally that transgenes situated on the Anopheles gambiae X chromosome are transcriptionally silenced in the male germline.

Conclusion

The data presented here support the hypothesis that the observed demasculinization of the Anopheles X chromosome is driven by X-chromosome inactivation in the male germline and by sexual antagonism. The demasculinization appears to be the consequence of a loss of male-biased expression, rather than a failure in the establishment or the extinction of male-biased genes.

Keywords:
Anopheles gambiae; demasculinization; germline x-chromosome inactivation; sexual antagonism; dosage compensation