Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta

Sex chromosome dosage compensation balances homogametic sex chromosome expression with autosomal expression in the heterogametic sex, leading to sex chromosome expression parity between the sexes. If compensation is incomplete, this can lead to expression imbalance and sex-biased gene expression. Re...

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Main Authors: Smith, Gilbert, Chen, Yun-Ru, Blissard, Gary W., Briscoe, Adriana D.
Format: Online
Language:English
Published: Oxford University Press 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971586/
id pubmed-3971586
recordtype oai_dc
spelling pubmed-39715862014-04-01 Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta Smith, Gilbert Chen, Yun-Ru Blissard, Gary W. Briscoe, Adriana D. Research Article Sex chromosome dosage compensation balances homogametic sex chromosome expression with autosomal expression in the heterogametic sex, leading to sex chromosome expression parity between the sexes. If compensation is incomplete, this can lead to expression imbalance and sex-biased gene expression. Recent work has uncovered an intriguing and variable pattern of dosage compensation across species that includes a lack of complete dosage compensation in ZW species compared with XY species. This has led to the hypothesis that ZW species do not require complete compensation or that complete compensation would negatively affect their fitness. To date, only one study, a study of the moth Bombyx mori, has discovered evidence for complete dosage compensation in a ZW species. We examined another moth species, Manduca sexta, using high-throughput sequencing to survey gene expression in the head tissue of males and females. We found dosage compensation to be complete in M. sexta with average expression between the Z chromosome in males and females being equal. When genes expressed at very low levels are removed by filtering, we found that average autosome expression was highly similar to average Z expression, suggesting that the majority of genes in M. sexta are completely dosage compensated. Further, this compensation was accompanied by sex-specific gene expression associated with important sexually dimorphic traits. We suggest that complete dosage compensation in ZW species might be more common than previously appreciated and linked to additional selective processes, such as sexual selection. More ZW and lepidopteran species should now be examined in a phylogenetic framework, to understand the evolution of dosage compensation. Oxford University Press 2014-02-19 /pmc/articles/PMC3971586/ /pubmed/24558255 http://dx.doi.org/10.1093/gbe/evu035 Text en © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Smith, Gilbert
Chen, Yun-Ru
Blissard, Gary W.
Briscoe, Adriana D.
spellingShingle Smith, Gilbert
Chen, Yun-Ru
Blissard, Gary W.
Briscoe, Adriana D.
Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
author_facet Smith, Gilbert
Chen, Yun-Ru
Blissard, Gary W.
Briscoe, Adriana D.
author_sort Smith, Gilbert
title Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
title_short Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
title_full Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
title_fullStr Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
title_full_unstemmed Complete Dosage Compensation and Sex-Biased Gene Expression in the Moth Manduca sexta
title_sort complete dosage compensation and sex-biased gene expression in the moth manduca sexta
description Sex chromosome dosage compensation balances homogametic sex chromosome expression with autosomal expression in the heterogametic sex, leading to sex chromosome expression parity between the sexes. If compensation is incomplete, this can lead to expression imbalance and sex-biased gene expression. Recent work has uncovered an intriguing and variable pattern of dosage compensation across species that includes a lack of complete dosage compensation in ZW species compared with XY species. This has led to the hypothesis that ZW species do not require complete compensation or that complete compensation would negatively affect their fitness. To date, only one study, a study of the moth Bombyx mori, has discovered evidence for complete dosage compensation in a ZW species. We examined another moth species, Manduca sexta, using high-throughput sequencing to survey gene expression in the head tissue of males and females. We found dosage compensation to be complete in M. sexta with average expression between the Z chromosome in males and females being equal. When genes expressed at very low levels are removed by filtering, we found that average autosome expression was highly similar to average Z expression, suggesting that the majority of genes in M. sexta are completely dosage compensated. Further, this compensation was accompanied by sex-specific gene expression associated with important sexually dimorphic traits. We suggest that complete dosage compensation in ZW species might be more common than previously appreciated and linked to additional selective processes, such as sexual selection. More ZW and lepidopteran species should now be examined in a phylogenetic framework, to understand the evolution of dosage compensation.
publisher Oxford University Press
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971586/
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