Developmental contexts of gene-regulatory evolution following whole genome duplication in salmonids
Abstract Whole genome duplication (WGD) events during early vertebrate evolution may have promoted phenotypic innovation by expanding the genetic material for functional diversification. However, their ancient origins obscure how gene regulation evolved during rediploidization, the process that generates duplicate genes and regulatory elements following WGD. Salmonids provide a unique window to these mechanisms, because they experienced a more recent autotetraploid WGD and remain at an earlier stage of rediploidization. Here we generated 771 multiomics datasets spanning embryonic and adult tissues in Atlantic salmon and rainbow trout to investigate the evolution of gene expression and regulatory elements. Our analyses show that regulatory evolution following the salmonid WGD was shaped by developmental and tissue-specific constraints known to act across vertebrate species. We identify a peak of within-genome regulatory constraint at the vertebrate phylotypic period, associated with the functional retention of duplicated enhancer pairs harbouring deeply conserved non-coding elements enriched in motifs for master developmental transcription factors. We further identify roles for enhancers and transposable elements in the expression divergence of duplicated genes. This study advances the understanding of regulatory evolution following WGD and offers an open resource supporting vertebrate comparative genomics and research applications in salmonid aquaculture and conservation.
Authors
- Garth R Ilsley (ORCID: https://orcid.org/0000-0001-9863-5802)
- Rose Ruiz Daniels (ORCID: https://orcid.org/0000-0002-6702-5304)
- Hugues Roest Crollius (ORCID: https://orcid.org/0000-0002-8209-173X)
- Erika Carrera‐García (ORCID: https://orcid.org/0000-0002-8270-3011)
- Diego Morata (ORCID: https://orcid.org/0000-0002-9751-2429)
- Simen R. Sandve (ORCID: https://orcid.org/0000-0003-4989-5311)
- Torgeir Rhoden Hvidsten (ORCID: https://orcid.org/0000-0001-6097-2539)
- Bojan Žunar (ORCID: https://orcid.org/0000-0002-6855-7222)
- Aline Perquis
- Alexandra Louis (ORCID: https://orcid.org/0000-0001-7032-5650)
- Camille Berthelot (ORCID: https://orcid.org/0000-0001-5054-2690)
- David Thybert (ORCID: https://orcid.org/0000-0001-7806-7318)
- Damir Baranas̆ić (ORCID: https://orcid.org/0000-0001-5948-0932)
- Marie-Odile Baudement (ORCID: https://orcid.org/0000-0003-2018-1657)
- Lars Grønvold (ORCID: https://orcid.org/0000-0001-5404-4285)
- Boris Lenhard (ORCID: https://orcid.org/0000-0002-1114-1509)
- Aurélien Brionne (ORCID: https://orcid.org/0009-0009-3301-3813)
- Peter W. Harrison (ORCID: https://orcid.org/0000-0002-4007-2899)
- Pooran Singh Dewari (ORCID: https://orcid.org/0000-0002-0256-0218)
- Tomasz Podgorniak (ORCID: https://orcid.org/0000-0002-9026-2308)
- Julien Bobe (ORCID: https://orcid.org/0000-0002-9355-8227)
- Daniel J. Macqueen (ORCID: https://orcid.org/0000-0001-8050-7722)
- Audrey Laurent (ORCID: https://orcid.org/0000-0002-7643-6017)
- Matthew Kent (ORCID: https://orcid.org/0000-0001-8822-8533)
- Gabriela Alejandra Merino (ORCID: https://orcid.org/0000-0002-0130-6226)
- Manu Kumar Gundappa (ORCID: https://orcid.org/0000-0003-4328-2178)
- Sigbjørn Lien (ORCID: https://orcid.org/0000-0002-5159-1950)
- François Giudicelli (ORCID: https://orcid.org/0000-0003-1320-2958)
- Yann Guiguen (ORCID: https://orcid.org/0000-0001-5464-6219)
- Gareth Gillard
- Tan Thi Nguyen
Institutions
- University of Stirling (GB)
- Centre National de la Recherche Scientifique (FR)
- European Bioinformatics Institute (GB)
- Roslin Institute (GB)
- Inserm (FR)
- Institut Pasteur (FR)
- University of Zagreb (HR)
- Université Paris Cité (FR)
- École Normale Supérieure - PSL (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Ruđer Bošković Institute (HR)
- Institut de Biologie de l'École Normale Supérieure (FR)
- Laboratoire de Physiologie et Génomique des Poissons (FR)
- Institut Cochin (FR)
- MRC London Institute of Medical Sciences (GB)
- Imperial College London (GB)
- Norwegian University of Life Sciences (NO)
- Wageningen University & Research (NL)
Publication Details
- Journal
- Nature Ecology & Evolution
- Published
- 2026-09-29
- DOI
- https://doi.org/10.1038/s41559-026-03171-6
- Primary Topic
- Chromosomal and Genetic Variations
- Type
- article
- Field-Weighted Citation Impact
- 0.00