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

TY - JOUR

T1 - Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow

AU - Papoli Yazdi, Homa

AU - Ravinet, Mark

AU - Rowe, Melissah

AU - Sætre, Glenn Peter

AU - Guldvog, Caroline

AU - Eroukhmanoff, Fabrice

AU - Marzal, Alfonso

AU - Magallanes, Sergio

AU - Runemark, Anna

N1 - Publisher Copyright: © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

PY - 2022

Y1 - 2022

N2 - 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.

AB - 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.

KW - gene expression

KW - hybridization

KW - mito-nuclear genes

KW - testis and transgressive expression

U2 - 10.1111/mec.16572

DO - 10.1111/mec.16572

M3 - Article

AN - SCOPUS:85133404467

SN - 0962-1083

VL - 31

SP - 4067

EP - 4077

JO - Molecular Ecology

JF - Molecular Ecology

IS - 15

ER -