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Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis

The magnitude and functional patterns of intraspecific transcriptional variation in the anophelines, including those of sex-biased genes underlying sex-specific traits relevant for malaria transmission, remain understudied. As a result, how changes in expression levels drive adaptation in these spec...

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Autores principales: Jayaswal, Vivek, Ndo, Cyrille, Ma, Hsiu-Ching, Clifton, Bryan D, Pombi, Marco, Cabrera, Kevin, Cohuet, Anna, Mouline, Karine, Diabaté, Abdoulaye, Dabiré, Roch, Ayala, Diego, Ranz, José M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8449828/
https://www.ncbi.nlm.nih.gov/pubmed/34432020
http://dx.doi.org/10.1093/gbe/evab199
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author Jayaswal, Vivek
Ndo, Cyrille
Ma, Hsiu-Ching
Clifton, Bryan D
Pombi, Marco
Cabrera, Kevin
Cohuet, Anna
Mouline, Karine
Diabaté, Abdoulaye
Dabiré, Roch
Ayala, Diego
Ranz, José M
author_facet Jayaswal, Vivek
Ndo, Cyrille
Ma, Hsiu-Ching
Clifton, Bryan D
Pombi, Marco
Cabrera, Kevin
Cohuet, Anna
Mouline, Karine
Diabaté, Abdoulaye
Dabiré, Roch
Ayala, Diego
Ranz, José M
author_sort Jayaswal, Vivek
collection PubMed
description The magnitude and functional patterns of intraspecific transcriptional variation in the anophelines, including those of sex-biased genes underlying sex-specific traits relevant for malaria transmission, remain understudied. As a result, how changes in expression levels drive adaptation in these species is poorly understood. We sequenced the female, male, and larval transcriptomes of three populations of Anopheles arabiensis from Burkina Faso. One-third of the genes were differentially expressed between populations, often involving insecticide resistance-related genes in a sample type-specific manner, and with the females showing the largest number of differentially expressed genes. At the genomic level, the X chromosome appears depleted of differentially expressed genes compared with the autosomes, chromosomes harboring inversions do not exhibit evidence for enrichment of such genes, and genes that are top contributors to functional enrichment patterns of population differentiation tend to be clustered in the genome. Further, the magnitude of variation for the sex expression ratio across populations did not substantially differ between male- and female-biased genes, except for some populations in which male-limited expressed genes showed more variation than their female counterparts. In fact, female-biased genes exhibited a larger level of interpopulation variation than male-biased genes, both when assayed in males and females. Beyond uncovering the extensive adaptive potential of transcriptional variation in An. Arabiensis, our findings suggest that the evolutionary rate of changes in expression levels on the X chromosome exceeds that on the autosomes, while pointing to female-biased genes as the most variable component of the An. Arabiensis transcriptome.
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spelling pubmed-84498282021-09-20 Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis Jayaswal, Vivek Ndo, Cyrille Ma, Hsiu-Ching Clifton, Bryan D Pombi, Marco Cabrera, Kevin Cohuet, Anna Mouline, Karine Diabaté, Abdoulaye Dabiré, Roch Ayala, Diego Ranz, José M Genome Biol Evol Research Article The magnitude and functional patterns of intraspecific transcriptional variation in the anophelines, including those of sex-biased genes underlying sex-specific traits relevant for malaria transmission, remain understudied. As a result, how changes in expression levels drive adaptation in these species is poorly understood. We sequenced the female, male, and larval transcriptomes of three populations of Anopheles arabiensis from Burkina Faso. One-third of the genes were differentially expressed between populations, often involving insecticide resistance-related genes in a sample type-specific manner, and with the females showing the largest number of differentially expressed genes. At the genomic level, the X chromosome appears depleted of differentially expressed genes compared with the autosomes, chromosomes harboring inversions do not exhibit evidence for enrichment of such genes, and genes that are top contributors to functional enrichment patterns of population differentiation tend to be clustered in the genome. Further, the magnitude of variation for the sex expression ratio across populations did not substantially differ between male- and female-biased genes, except for some populations in which male-limited expressed genes showed more variation than their female counterparts. In fact, female-biased genes exhibited a larger level of interpopulation variation than male-biased genes, both when assayed in males and females. Beyond uncovering the extensive adaptive potential of transcriptional variation in An. Arabiensis, our findings suggest that the evolutionary rate of changes in expression levels on the X chromosome exceeds that on the autosomes, while pointing to female-biased genes as the most variable component of the An. Arabiensis transcriptome. Oxford University Press 2021-08-25 /pmc/articles/PMC8449828/ /pubmed/34432020 http://dx.doi.org/10.1093/gbe/evab199 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Jayaswal, Vivek
Ndo, Cyrille
Ma, Hsiu-Ching
Clifton, Bryan D
Pombi, Marco
Cabrera, Kevin
Cohuet, Anna
Mouline, Karine
Diabaté, Abdoulaye
Dabiré, Roch
Ayala, Diego
Ranz, José M
Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title_full Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title_fullStr Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title_full_unstemmed Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title_short Intraspecific Transcriptome Variation and Sex-Biased Expression in Anopheles arabiensis
title_sort intraspecific transcriptome variation and sex-biased expression in anopheles arabiensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8449828/
https://www.ncbi.nlm.nih.gov/pubmed/34432020
http://dx.doi.org/10.1093/gbe/evab199
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