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

Papoli Yazdi, Homa LU ; Ravinet, Mark ; Rowe, Melissah ; Sætre, Glenn Peter ; Guldvog, Caroline ; Eroukhmanoff, Fabrice ; Marzal, Alfonso ; Magallanes, Sergio and Runemark, Anna LU (2022) In Molecular Ecology 31(15). p.4067-4077
Abstract

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F1 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... (More)

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F1 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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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
gene expression, hybridization, mito-nuclear genes, testis and transgressive expression
in
Molecular Ecology
volume
31
issue
15
pages
11 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:85133404467
  • pmid:35726533
ISSN
0962-1083
DOI
10.1111/mec.16572
language
English
LU publication?
yes
id
c97b0a49-8a59-47df-b1bb-134eb35be44d
date added to LUP
2022-09-23 15:20:04
date last changed
2024-06-12 04:13:40
@article{c97b0a49-8a59-47df-b1bb-134eb35be44d,
  abstract     = {{<p>Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F<sub>1</sub> 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.</p>}},
  author       = {{Papoli Yazdi, Homa and Ravinet, Mark and Rowe, Melissah and Sætre, Glenn Peter and Guldvog, Caroline and Eroukhmanoff, Fabrice and Marzal, Alfonso and Magallanes, Sergio and Runemark, Anna}},
  issn         = {{0962-1083}},
  keywords     = {{gene expression; hybridization; mito-nuclear genes; testis and transgressive expression}},
  language     = {{eng}},
  number       = {{15}},
  pages        = {{4067--4077}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Ecology}},
  title        = {{Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow}},
  url          = {{http://dx.doi.org/10.1111/mec.16572}},
  doi          = {{10.1111/mec.16572}},
  volume       = {{31}},
  year         = {{2022}},
}