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

Francesco Papa, Nikolai Windbichler, Robert M. Waterhouse, Alessia Cagnetti, Rocco D'Amato, Tania Persampieri, Mara K.N. Lawniczak, Tony Nolan, Philippos Aris Papathanos*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

40 Scopus citations


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.

Original languageAmerican English
Pages (from-to)1536-1548
Number of pages13
JournalGenome Research
Issue number9
StatePublished - Sep 2017
Externally publishedYes

Bibliographical note

Funding Information:
We thank Scott Cornman, Sara Mitchell, Adam Jenkins, Michael Riehle, Craig Wilding, Xiofan Zhou, and Jose Ribeiro for providing us with manual community annotations of An. gambiae gene functions, and Paul Howell at the MR4/BEI for support on rearing of the mosquito species. This study has received funding from the European Union’s Seventh Framework Programme (FP7 2007– 2013 Infravec) under the GA no. 228421. This study was also funded by the European Union’s Seventh Framework Programme (FP7 2007–2013) Marie Curie Actions cofund (Project I-Move) under GA no. 267232. This study was funded in part by a grant from the Foundation for the National Institutes of Health through the Vector-Based Control of Transmission: Discovery Research (VCTR) program of the Grand Challenges in Global Health initiative of the Bill & Melinda Gates Foundation. P.A.P. was supported by a Rita Levi Montalcini award from the Ministry of Education, University and Research (MIUR – D.M. no. 79 04.02.2014). This study was also funded by the European Research Council under the European Union’s Seventh Framework Programme ERC grant no. 335724 awarded to N.W. R.M.W. was supported by Marie Curie International Outgoing Fellowship (European Commission) PIOF-GA-2011-303312. M.K.N.L. was supported by a Medical Research Council (MRC) Career Development Award (G1100339) and by the Wellcome Trust (098051). R.M.W. was supported by Swiss National Science Foundation grant PP00P3_170664.

Publisher Copyright:
© 2017 Papa et al.


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