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

    • 1Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy;
    • 2Department of Life Sciences, Imperial College London, SW7 2AZ London, United Kingdom;
    • 3University of Geneva Medical School and Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland;
    • 4Massachusetts Institute of Technology and the Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02139, USA;
    • 5Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland;
    • 6Polo d'Innovazione di Genomica, Genetica e Biologia, 06132 Perugia, Italy;
    • 7Welcome Trust Sanger Institute, CB10 1SA Hinxton, United Kingdom
Published July 26, 2017. https://doi.org/10.1101/gr.217216.116
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cover of Genome Research Vol 36 Issue 7
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Abstract

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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