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Genome Res. 2017 Sep;27(9):1536-1548. doi: 10.1101/gr.217216.116. Epub 2017 Jul 26.

Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes.

Author information

Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy.
Department of Life Sciences, Imperial College London, SW7 2AZ London, United Kingdom.
University of Geneva Medical School and Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
Massachusetts Institute of Technology and the Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02139, USA.
Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland.
Polo d'Innovazione di Genomica, Genetica e Biologia, 06132 Perugia, Italy.
Welcome Trust Sanger Institute, CB10 1SA Hinxton, United Kingdom.


Understanding how phenotypic differences between males and females arise from the sex-biased expression of nearly identical genomes can reveal important insights into the biology and evolution of a species. Among Anopheles mosquito species, these phenotypic differences include vectorial capacity, as it is only females that blood feed and thus transmit human malaria. Here, we use RNA-seq data from multiple tissues of four vector species spanning the Anopheles phylogeny to explore the genomic and evolutionary properties of sex-biased genes. We find that, in these mosquitoes, in contrast to what has been found in many other organisms, female-biased genes are more rapidly evolving in sequence, expression, and genic turnover than male-biased genes. Our results suggest that this atypical pattern may be due to the combination of sex-specific life history challenges encountered by females, such as blood feeding. Furthermore, female propensity to mate only once in nature in male swarms likely diminishes sexual selection of post-reproductive traits related to sperm competition among males. We also develop a comparative framework to systematically explore tissue- and sex-specific splicing to document its conservation throughout the genus and identify a set of candidate genes for future functional analyses of sex-specific isoform usage. Finally, our data reveal that the deficit of male-biased genes on the X Chromosomes in Anopheles is a conserved feature in this genus and can be directly attributed to chromosome-wide transcriptional regulation that de-masculinizes the X in male reproductive tissues.

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