Demasculinization of the Anopheles gambiae X chromosome

Kalle Magnusson, Gareth J. Lycett, Antonio M. Mendes, Amy Lynd, Philippos Aris Papathanos, Andrea Crisanti, Nikolai Windbichler*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

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.

Original languageAmerican English
Article number69
JournalBMC Evolutionary Biology
Volume12
Issue number1
DOIs
StatePublished - 2012
Externally publishedYes

Bibliographical note

Funding Information:
We thank Tony Nolan for critically reading the manuscript. We thank Miriam Menicheli and Ann Hall for technical support. We also thank Lucy Collyns for secretarial help. This work was supported by a Grant of the Foundation for the National Institutes of Health through the Grand Challenges in Global Health initiative (www.grandchallenges.org/) as well as by a Grant of the BBSRC (www.bbsrc.ac.uk) awarded to AC. Part of this work, performed by GL and AL, was funded through the European Commission FP7 Collaborative project TransMalariaBloc (HEALTH-F3-2008-223736) and a BBSRC grant (BB/ F021933/1) awarded to GL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Keywords

  • Anopheles gambiae
  • demasculinization
  • dosage compensation
  • germline x-chromosome inactivation
  • sexual antagonism

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