Gene expression differentiation in the reproductive tissues of Drosophila willistoni subspecies and their hybrids.

dosage compensation hybrid dysfunction neo-X chromosome regulatory evolution transcriptome divergence

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
07 2023
Historique:
revised: 11 03 2023
received: 23 07 2022
accepted: 27 03 2023
medline: 28 6 2023
pubmed: 1 4 2023
entrez: 31 3 2023
Statut: ppublish

Résumé

Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about what genes and pathways underlie hybrid dysfunction. In Drosophila hybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation in Drosophila willistoni and analyse the patterns of transcriptome divergence between two allopatrically evolved D. willistoni subspecies, their male sterile and female fertile hybrid progeny across testis, male accessory gland, and ovary. Patterns of transcriptome divergence and modes of regulatory evolution were tissue-specific. Despite no indication for cell-type differences in hybrid testis, this tissue exhibited the largest magnitude of expression differentiation between subspecies and between parentals and hybrids. No evidence for anomalous dosage compensation in hybrid male tissues was detected nor was a differential role for the neo- and the ancestral arms of the D. willistoni X chromosome. Compared to the autosomes, the X chromosome appeared enriched for transgressively expressed genes in testis despite being the least differentiated in expression between subspecies. Evidence for fine genome clustering of transgressively expressed genes suggests a role of chromatin structure on hybrid gene misregulation. Lastly, transgressively expressed genes in the testis of the sterile male progeny were enriched for GO terms not typically associated with sperm function, instead hinting at anomalous development of the reproductive tissue. Our thorough tissue-level portrait of transcriptome differentiation between recently diverged D. willistoni subspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation.

Identifiants

pubmed: 37000122
doi: 10.1111/mec.16941
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

3605-3623

Informations de copyright

© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

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Auteurs

José M Ranz (JM)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Alwyn C Go (AC)

Department of Biology, University of Winnipeg, Winnipeg, Manitoba, Canada.

Pablo M González (PM)

Unidad de Genómica Avanzada (Langebio), CINVESTAV, Irapuato GTO, Mexico.

Bryan D Clifton (BD)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Suzanne Gomes (S)

Department of Biology, University of Winnipeg, Winnipeg, Manitoba, Canada.

Amirali Jaberyzadeh (A)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Amanda Woodbury (A)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Carolus Chan (C)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Kania A Gandasetiawan (KA)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Suvini Jayasekera (S)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Chelsea Gaudreau (C)

Department of Biology, University of Winnipeg, Winnipeg, Manitoba, Canada.

Hsiu-Ching Ma (HC)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.

Victor M Salceda (VM)

Department of Ecology and Evolutionary Biology, University of California Irvine, California, USA.
Departamento de Biología, Instituto Nacional de Investigaciones Nucleares, Ocoyoacac, Mexico.

Cei Abreu-Goodger (C)

Unidad de Genómica Avanzada (Langebio), CINVESTAV, Irapuato GTO, Mexico.

Alberto Civetta (A)

Department of Biology, University of Winnipeg, Winnipeg, Manitoba, Canada.

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