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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

1
Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy.
2
Department of Life Sciences, Imperial College London, SW7 2AZ London, United Kingdom.
3
University of Geneva Medical School and Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
4
Massachusetts Institute of Technology and the Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02139, USA.
5
Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland.
6
Polo d'Innovazione di Genomica, Genetica e Biologia, 06132 Perugia, Italy.
7
Welcome Trust Sanger Institute, CB10 1SA Hinxton, United Kingdom.

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.

PMID:
28747381
PMCID:
PMC5580713
DOI:
10.1101/gr.217216.116
[Indexed for MEDLINE]
Free PMC Article

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