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

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...

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Autores principales: Papa, Francesco, Windbichler, Nikolai, Waterhouse, Robert M., Cagnetti, Alessia, D'Amato, Rocco, Persampieri, Tania, Lawniczak, Mara K.N., Nolan, Tony, Papathanos, Philippos Aris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5580713/
https://www.ncbi.nlm.nih.gov/pubmed/28747381
http://dx.doi.org/10.1101/gr.217216.116
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author Papa, Francesco
Windbichler, Nikolai
Waterhouse, Robert M.
Cagnetti, Alessia
D'Amato, Rocco
Persampieri, Tania
Lawniczak, Mara K.N.
Nolan, Tony
Papathanos, Philippos Aris
author_facet Papa, Francesco
Windbichler, Nikolai
Waterhouse, Robert M.
Cagnetti, Alessia
D'Amato, Rocco
Persampieri, Tania
Lawniczak, Mara K.N.
Nolan, Tony
Papathanos, Philippos Aris
author_sort Papa, Francesco
collection PubMed
description 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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spelling pubmed-55807132017-09-14 Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes Papa, Francesco Windbichler, Nikolai Waterhouse, Robert M. Cagnetti, Alessia D'Amato, Rocco Persampieri, Tania Lawniczak, Mara K.N. Nolan, Tony Papathanos, Philippos Aris Genome Res Research 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. Cold Spring Harbor Laboratory Press 2017-09 /pmc/articles/PMC5580713/ /pubmed/28747381 http://dx.doi.org/10.1101/gr.217216.116 Text en © 2017 Papa et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ 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/.
spellingShingle Research
Papa, Francesco
Windbichler, Nikolai
Waterhouse, Robert M.
Cagnetti, Alessia
D'Amato, Rocco
Persampieri, Tania
Lawniczak, Mara K.N.
Nolan, Tony
Papathanos, Philippos Aris
Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title_full Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title_fullStr Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title_full_unstemmed Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title_short Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes
title_sort rapid evolution of female-biased genes among four species of anopheles malaria mosquitoes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5580713/
https://www.ncbi.nlm.nih.gov/pubmed/28747381
http://dx.doi.org/10.1101/gr.217216.116
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