Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
- Francesco Papa1,
- Nikolai Windbichler2,
- Robert M. Waterhouse3,4,5,
- Alessia Cagnetti1,6,
- Rocco D'Amato1,
- Tania Persampieri1,6,
- Mara K.N. Lawniczak7,
- Tony Nolan2 and
- Philippos Aris Papathanos1
- 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
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.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.217216.116.
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Freely available online through the Genome Research Open Access option.
- Received October 17, 2016.
- Accepted July 18, 2017.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
