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Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

BACKGROUND: Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-l...

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Autores principales: Chauhan, Pallavi, Wellenreuther, Maren, Hansson, Bengt
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5131402/
https://www.ncbi.nlm.nih.gov/pubmed/27905879
http://dx.doi.org/10.1186/s12864-016-3334-6
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author Chauhan, Pallavi
Wellenreuther, Maren
Hansson, Bengt
author_facet Chauhan, Pallavi
Wellenreuther, Maren
Hansson, Bengt
author_sort Chauhan, Pallavi
collection PubMed
description BACKGROUND: Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict. RESULTS: The de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph. CONCLUSIONS: This is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3334-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-51314022016-12-12 Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression Chauhan, Pallavi Wellenreuther, Maren Hansson, Bengt BMC Genomics Research Article BACKGROUND: Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict. RESULTS: The de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph. CONCLUSIONS: This is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3334-6) contains supplementary material, which is available to authorized users. BioMed Central 2016-12-01 /pmc/articles/PMC5131402/ /pubmed/27905879 http://dx.doi.org/10.1186/s12864-016-3334-6 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Chauhan, Pallavi
Wellenreuther, Maren
Hansson, Bengt
Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title_full Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title_fullStr Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title_full_unstemmed Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title_short Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression
title_sort transcriptome profiling in the damselfly ischnura elegans identifies genes with sex-biased expression
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5131402/
https://www.ncbi.nlm.nih.gov/pubmed/27905879
http://dx.doi.org/10.1186/s12864-016-3334-6
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