4.7 Article

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

Journal

GENOME RESEARCH
Volume 27, Issue 9, Pages 1536-1548

Publisher

COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT
DOI: 10.1101/gr.217216.116

Keywords

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Funding

  1. European Union [228421]
  2. European Union's Seventh Framework Programme (FP7) Marie Curie Actions cofund (Project I-Move) [267232]
  3. 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
  4. Rita Levi Montalcini award from the Ministry of Education, University and Research (MIUR) [79 04.02.2014]
  5. European Research Council under the European Union's Seventh Framework Programme ERC [335724]
  6. Marie Curie International Outgoing Fellowship (European Commission) [PIOF-GA-2011-303312]
  7. Medical Research Council (MRC) Career Development Award [G1100339]
  8. Wellcome Trust [098051]
  9. Swiss National Science Foundation grant [PPOOP3_170664]
  10. Medical Research Council [G1100339] Funding Source: researchfish
  11. European Research Council (ERC) [335724] Funding Source: European Research Council (ERC)
  12. MRC [G1100339] Funding Source: UKRI

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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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