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

43 Scopus citations

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.

Original languageAmerican English
Pages (from-to)1536-1548
Number of pages13
JournalGenome Research
Volume27
Issue number9
DOIs
StatePublished - Sep 2017
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2017 Papa et al.

Fingerprint

Dive into the research topics of 'Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes'. Together they form a unique fingerprint.

Cite this