Why are male malaria parasites in such a rush?: Sex-specific evolution and host-parasite interactions.
BACKGROUND
Disease-causing organisms are notorious for fast rates of molecular evolution and the ability to adapt rapidly to changes in their ecology. Sex plays a key role in evolution, and recent studies, in humans and other multicellular organisms, document that genes expressed principally or exclusively in males exhibit the fastest rates of adaptive evolution. However, despite the importance of sexual reproduction for many unicellular taxa, sex-biased gene expression and its evolutionary implications have been overlooked.


METHODS
We analyse genomic data from multiple malaria parasite (Plasmodium) species and proteomic data sets from different parasite life cycle stages.


RESULTS
The accelerated evolution of male-biased genes has only been examined in multicellular taxa, but our analyses reveal that accelerated evolution in genes with male-specific expression is also a feature of unicellular organisms. This 'fast-male' evolution is adaptive and likely facilitated by the male-biased sex ratio of gametes in the mating pool. Furthermore, we propose that the exceptional rates of evolution we observe are driven by interactions between males and host immune responses.


CONCLUSIONS
We reveal a novel form of host-parasite coevolution that enables parasites to evade host immune responses that negatively impact upon fertility. The identification of parasite genes with accelerated evolution has important implications for the identification of drug and vaccine targets. Specifically, vaccines targeting males will be more vulnerable to parasite evolution than those targeting females or both sexes.
Leiden Malaria Research Group, Department of Parasitology, LUMC, Albinusdreef 2, 2333 ZA Leiden, The Netherlands; Centre for Immunity, Infection and Evolution, Institutes of Evolution, Infection and Immunity, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK; Division of Infection and Immunity, Institute of Biomedical Life Sciences & Wellcome Centre for Molecular Parasitology, University of Glasgow, Glasgow G12 8TA, UK; Department of Bioinformatics, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawinskiego 5a, 02-106 Warszawa, Poland.
Shahid M
SM
Khan
Sarah E
SE
Reece
Andrew P
AP
Waters
Chris J
CJ
Janse
Szymon
S
Kaczanowski
Plasmodium; gene expression; host–parasite coevolution; sex-specific selection