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Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F(1) hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a sta...

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Autores principales: Papoli Yazdi, Homa, Ravinet, Mark, Rowe, Melissah, Sætre, Glenn‐Peter, Guldvog, Caroline Ø., Eroukhmanoff, Fabrice, Marzal, Alfonso, Magallanes, Sergio, Runemark, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9542029/
https://www.ncbi.nlm.nih.gov/pubmed/35726533
http://dx.doi.org/10.1111/mec.16572
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author Papoli Yazdi, Homa
Ravinet, Mark
Rowe, Melissah
Sætre, Glenn‐Peter
Guldvog, Caroline Ø.
Eroukhmanoff, Fabrice
Marzal, Alfonso
Magallanes, Sergio
Runemark, Anna
author_facet Papoli Yazdi, Homa
Ravinet, Mark
Rowe, Melissah
Sætre, Glenn‐Peter
Guldvog, Caroline Ø.
Eroukhmanoff, Fabrice
Marzal, Alfonso
Magallanes, Sergio
Runemark, Anna
author_sort Papoli Yazdi, Homa
collection PubMed
description Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F(1) hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break‐up of co‐evolved cis‐ and trans‐regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows—2530 genes (22% of testis genes tested for inheritance) exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over‐dominantly expressed in Italian sparrow testis, suggesting that selection on key functions has moulded the hybrid Italian sparrow transcriptome.
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spelling pubmed-95420292022-10-14 Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow Papoli Yazdi, Homa Ravinet, Mark Rowe, Melissah Sætre, Glenn‐Peter Guldvog, Caroline Ø. Eroukhmanoff, Fabrice Marzal, Alfonso Magallanes, Sergio Runemark, Anna Mol Ecol ORIGINAL ARTICLES Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F(1) hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break‐up of co‐evolved cis‐ and trans‐regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows—2530 genes (22% of testis genes tested for inheritance) exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over‐dominantly expressed in Italian sparrow testis, suggesting that selection on key functions has moulded the hybrid Italian sparrow transcriptome. John Wiley and Sons Inc. 2022-07-04 2022-08 /pmc/articles/PMC9542029/ /pubmed/35726533 http://dx.doi.org/10.1111/mec.16572 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle ORIGINAL ARTICLES
Papoli Yazdi, Homa
Ravinet, Mark
Rowe, Melissah
Sætre, Glenn‐Peter
Guldvog, Caroline Ø.
Eroukhmanoff, Fabrice
Marzal, Alfonso
Magallanes, Sergio
Runemark, Anna
Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title_full Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title_fullStr Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title_full_unstemmed Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title_short Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
title_sort extensive transgressive gene expression in testis but not ovary in the homoploid hybrid italian sparrow
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9542029/
https://www.ncbi.nlm.nih.gov/pubmed/35726533
http://dx.doi.org/10.1111/mec.16572
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