Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners

ABSTRACT Allochrony is a form of reproductive isolation characterized by differences in the timing of spawning and may play a crucial role in the genetic and phenotypic divergence within species. The Atlantic lumpfish (Cyclopterus lumpus) is known to spawn in spring and autumn. However, the role of...

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Main Authors: Mathilde Horaud, Núria Raventós, Kim Præbel, Carles Galià‐Camps, Cinta Pegueroles, Carlos Carreras, Marta Pascual, Victor M. Tuset, Shripathi Bhat, Arve Lynghammar
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Ecology and Evolution
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Online Access:https://doi.org/10.1002/ece3.70946
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author Mathilde Horaud
Núria Raventós
Kim Præbel
Carles Galià‐Camps
Cinta Pegueroles
Carlos Carreras
Marta Pascual
Victor M. Tuset
Shripathi Bhat
Arve Lynghammar
author_facet Mathilde Horaud
Núria Raventós
Kim Præbel
Carles Galià‐Camps
Cinta Pegueroles
Carlos Carreras
Marta Pascual
Victor M. Tuset
Shripathi Bhat
Arve Lynghammar
author_sort Mathilde Horaud
collection DOAJ
description ABSTRACT Allochrony is a form of reproductive isolation characterized by differences in the timing of spawning and may play a crucial role in the genetic and phenotypic divergence within species. The Atlantic lumpfish (Cyclopterus lumpus) is known to spawn in spring and autumn. However, the role of allochrony on the genomic structure of this species has not been addressed. Here, by combining whole genome sequencing data and otolith shape of 64 specimens, we explore the evolutionary drivers of divergence in Atlantic lumpfish, focusing on spring and autumn spawners sampled at two well‐separated spawning grounds along the Norwegian coast. Overall, we identified pronounced genomic and morphologic differences between the two spawning groups. Genomic differences between the two groups were concentrated in three chromosomes, with a region of chromosome 1 encompassing the same single nucleotide polymorphisms (SNPs) driving differential season spawning for both localities, suggesting parallel responses. The functional analysis of the SNPs in this region revealed genes associated with responses to environmental stressors, possibly adaptations to seasonal variations at high latitudes. The morphological analysis of otoliths supported these findings, showing differences compatible with adaptations to seasonal light availability. The presence of genomic islands of divergence, alongside a general lack of differentiation across the mitochondrial genome, suggest recent and rapid selection processes potentially modulated by ongoing gene flow. This study underscores the importance of considering temporal genetic structures, particularly for species with bimodal spawning time, in conservation and management strategies to prevent overexploitation and optimize breeding programs.
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spelling doaj-art-3e1d61580cf14965a17fb9cc8fdfdce42025-08-20T03:13:50ZengWileyEcology and Evolution2045-77582025-02-01152n/an/a10.1002/ece3.70946Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn SpawnersMathilde Horaud0Núria Raventós1Kim Præbel2Carles Galià‐Camps3Cinta Pegueroles4Carlos Carreras5Marta Pascual6Victor M. Tuset7Shripathi Bhat8Arve Lynghammar9Faculty of Biosciences, Fisheries and Economics, The Norwegian College of Fishery Science UiT The Arctic University of Norway Tromsø NorwayCentre d'Estudis Avançats de Blanes (CEAB‐CSIC) Blanes SpainFaculty of Biosciences, Fisheries and Economics, The Norwegian College of Fishery Science UiT The Arctic University of Norway Tromsø NorwayCentre d'Estudis Avançats de Blanes (CEAB‐CSIC) Blanes SpainDepartment of Genetics, Microbiology and Statistics University of Barcelona (UB) Barcelona SpainDepartment of Genetics, Microbiology and Statistics University of Barcelona (UB) Barcelona SpainDepartment of Genetics, Microbiology and Statistics University of Barcelona (UB) Barcelona SpainUnidad Asociada ULPGC‐CSIC, Instituto de Oceanografía y Cambio Global, IOCAG Universidad de las Palmas de Gran Canaria Telde Gran Canaria, Canary Islands SpainFaculty of Biosciences, Fisheries and Economics, The Norwegian College of Fishery Science UiT The Arctic University of Norway Tromsø NorwayFaculty of Biosciences, Fisheries and Economics, The Norwegian College of Fishery Science UiT The Arctic University of Norway Tromsø NorwayABSTRACT Allochrony is a form of reproductive isolation characterized by differences in the timing of spawning and may play a crucial role in the genetic and phenotypic divergence within species. The Atlantic lumpfish (Cyclopterus lumpus) is known to spawn in spring and autumn. However, the role of allochrony on the genomic structure of this species has not been addressed. Here, by combining whole genome sequencing data and otolith shape of 64 specimens, we explore the evolutionary drivers of divergence in Atlantic lumpfish, focusing on spring and autumn spawners sampled at two well‐separated spawning grounds along the Norwegian coast. Overall, we identified pronounced genomic and morphologic differences between the two spawning groups. Genomic differences between the two groups were concentrated in three chromosomes, with a region of chromosome 1 encompassing the same single nucleotide polymorphisms (SNPs) driving differential season spawning for both localities, suggesting parallel responses. The functional analysis of the SNPs in this region revealed genes associated with responses to environmental stressors, possibly adaptations to seasonal variations at high latitudes. The morphological analysis of otoliths supported these findings, showing differences compatible with adaptations to seasonal light availability. The presence of genomic islands of divergence, alongside a general lack of differentiation across the mitochondrial genome, suggest recent and rapid selection processes potentially modulated by ongoing gene flow. This study underscores the importance of considering temporal genetic structures, particularly for species with bimodal spawning time, in conservation and management strategies to prevent overexploitation and optimize breeding programs.https://doi.org/10.1002/ece3.70946allochronyatlantique lumpfishotolith shapespawning groundswhole genome sequencing
spellingShingle Mathilde Horaud
Núria Raventós
Kim Præbel
Carles Galià‐Camps
Cinta Pegueroles
Carlos Carreras
Marta Pascual
Victor M. Tuset
Shripathi Bhat
Arve Lynghammar
Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
Ecology and Evolution
allochrony
atlantique lumpfish
otolith shape
spawning grounds
whole genome sequencing
title Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
title_full Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
title_fullStr Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
title_full_unstemmed Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
title_short Allochrony in Atlantic Lumpfish: Genomic and Otolith Shape Divergence Between Spring and Autumn Spawners
title_sort allochrony in atlantic lumpfish genomic and otolith shape divergence between spring and autumn spawners
topic allochrony
atlantique lumpfish
otolith shape
spawning grounds
whole genome sequencing
url https://doi.org/10.1002/ece3.70946
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