Decay of sexual trait genes in an asexual parasitoid wasp
Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral...
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Published in | Genome biology and evolution Vol. 8; no. 12; pp. evw273 - 3695 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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England
Oxford University Press
01.12.2016
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Abstract | Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineage does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes. Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed study of the genomics of neutral and selected trait decay. |
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AbstractList | Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineage does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes. Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed study of the genomics of neutral and selected trait decay. Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineage does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes. Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed study of the genomics of neutral and selected trait decay.Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineage does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes. Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed study of the genomics of neutral and selected trait decay. Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineage does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes . Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed study of the genomics of neutral and selected trait decay. |
Author | Petersen, Malte Frank, Jeroen Ziesmann, Tanja Niehuis, Oliver Knijff, Peter de Anvar, Yahya Bast, Jens Kraaijeveld, Ken Schmitz, Arnoud Ellers, Jacintha Dunnen, Johan T. den Wilbrandt, Jeanne |
AuthorAffiliation | 5 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands 3 Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland 4 Zoological Research Museum Alexander Koenig, Center for Molecular Biodiversity Research, Bonn, Germany 1 Animal Ecology, Department of Ecological Sciences, VU University Amsterdam, The Netherlands 2 Leiden Genome Technology Center, Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands |
AuthorAffiliation_xml | – name: 3 Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland – name: 4 Zoological Research Museum Alexander Koenig, Center for Molecular Biodiversity Research, Bonn, Germany – name: 5 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – name: 2 Leiden Genome Technology Center, Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – name: 1 Animal Ecology, Department of Ecological Sciences, VU University Amsterdam, The Netherlands |
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Copyright | The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2017 |
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Keywords | Leptopilina clavipes parthenogenesis deleterious variants sexual trait decay Wolbachia |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Associate editor: Sarah Schaack Data deposition: The data for this project can be browsed and downloaded at http://parasitoids.labs.vu.nl/. This Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession JUFY00000000. The version described in this paper is version JUFY01000000. Fastq files containing the Illumina GAIIx sequence reads for the sexual lineage are available at Dryad: doi: 10.5061/dryad.k3bh40bg. The transcriptome assembly has been released as part of the 1KITE project: http://www.ncbi.nlm.nih.gov/bioproject/219570. |
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SubjectTerms | Animals Female Genes, Insect Male Mutation Phenotype Phylogeny Polymorphism, Single Nucleotide Reproduction, Asexual Wasps - genetics Wasps - physiology |
Title | Decay of sexual trait genes in an asexual parasitoid wasp |
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