Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.

Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions...

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Main Authors: Alfredo Rago, John H Werren, John K Colbourne
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008518
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spelling doaj-2b0182ce897a4d91bf07256e580274222021-04-21T14:21:30ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-01-01161e100851810.1371/journal.pgen.1008518Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.Alfredo RagoJohn H WerrenJohn K ColbourneSexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.https://doi.org/10.1371/journal.pgen.1008518
collection DOAJ
language English
format Article
sources DOAJ
author Alfredo Rago
John H Werren
John K Colbourne
spellingShingle Alfredo Rago
John H Werren
John K Colbourne
Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
PLoS Genetics
author_facet Alfredo Rago
John H Werren
John K Colbourne
author_sort Alfredo Rago
title Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
title_short Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
title_full Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
title_fullStr Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
title_full_unstemmed Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis.
title_sort sex biased expression and co-expression networks in development, using the hymenopteran nasonia vitripennis.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2020-01-01
description Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.
url https://doi.org/10.1371/journal.pgen.1008518
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