Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae

ABSTRACT While acquiring age information is crucial for efficient stock management and biodiversity conservation, traditional aging methods fail to offer a universal, non‐invasive, and precise way of estimating a wild animal's age. DNA methylation from tissue DNA (tDNA) was recently proposed as...

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Main Authors: Eliot Ruiz, Fabien Leprieur, Gérard Sposito, Martina Lüthi, Michel Schmidlin, Jacques Panfili, Loïc Pellissier, Camille Albouy
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Ecology and Evolution
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Online Access:https://doi.org/10.1002/ece3.70645
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author Eliot Ruiz
Fabien Leprieur
Gérard Sposito
Martina Lüthi
Michel Schmidlin
Jacques Panfili
Loïc Pellissier
Camille Albouy
author_facet Eliot Ruiz
Fabien Leprieur
Gérard Sposito
Martina Lüthi
Michel Schmidlin
Jacques Panfili
Loïc Pellissier
Camille Albouy
author_sort Eliot Ruiz
collection DOAJ
description ABSTRACT While acquiring age information is crucial for efficient stock management and biodiversity conservation, traditional aging methods fail to offer a universal, non‐invasive, and precise way of estimating a wild animal's age. DNA methylation from tissue DNA (tDNA) was recently proposed as a method to overcome these issues and showed more accurate results than telomere‐length‐based age assessments. Here, we used environmental DNA (eDNA) for the first time as a template for age estimation, focusing on the larval phase (10–24 days post‐hatch) of cultured Dicentrarchus labrax (seabass), a species of major economic and conservation interest. Using third‐generation sequencing, we were able to directly detect various modification types (e.g., cytosine and adenosine methylation in all contexts) across the whole genome using amplification‐free nanopore sequencing. However, aging sites were only present in the mitogenome, which could be a specific feature of eDNA methylation or the consequence of better DNA protection within mitochondria. By considering qualitative and quantitative information about aging sites according to an objective model selection framework, our epigenetic clock reached a cross‐validated accuracy of 2.6 days (Median Absolute Error). Such performances are higher than those of previous clocks, notably for adult seabass even when scaling MAE to the age range, which could be linked to a more dynamic epigenome during early life stages. Overall, our pilot study proposes new methods to determine the potential of eDNA for simultaneous age and biodiversity assessments, although robust validation of our preliminary results along with methodological developments are needed before field applications can be envisaged.
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spelling doaj-art-ad2af7099f9b4fa391f3a151de0fd8842025-08-20T03:51:30ZengWileyEcology and Evolution2045-77582025-02-01152n/an/a10.1002/ece3.70645Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish LarvaeEliot Ruiz0Fabien Leprieur1Gérard Sposito2Martina Lüthi3Michel Schmidlin4Jacques Panfili5Loïc Pellissier6Camille Albouy7MARBEC, Univ Montpellier, IRD, IFREMER, CNRS Montpellier FranceMARBEC, Univ Montpellier, IRD, IFREMER, CNRS Montpellier FranceMediterranean Coastal Environment Station University of Montpellier Sète FranceDepartment of Environmental Systems Science, Ecosystems and Landscape Evolution, Institute of Terrestrial Ecosystems ETH Zürich Zürich SwitzerlandDepartment of Environmental Systems Science, Ecosystems and Landscape Evolution, Institute of Terrestrial Ecosystems ETH Zürich Zürich SwitzerlandMARBEC, Univ Montpellier, IRD, IFREMER, CNRS Montpellier FranceDepartment of Environmental Systems Science, Ecosystems and Landscape Evolution, Institute of Terrestrial Ecosystems ETH Zürich Zürich SwitzerlandDepartment of Environmental Systems Science, Ecosystems and Landscape Evolution, Institute of Terrestrial Ecosystems ETH Zürich Zürich SwitzerlandABSTRACT While acquiring age information is crucial for efficient stock management and biodiversity conservation, traditional aging methods fail to offer a universal, non‐invasive, and precise way of estimating a wild animal's age. DNA methylation from tissue DNA (tDNA) was recently proposed as a method to overcome these issues and showed more accurate results than telomere‐length‐based age assessments. Here, we used environmental DNA (eDNA) for the first time as a template for age estimation, focusing on the larval phase (10–24 days post‐hatch) of cultured Dicentrarchus labrax (seabass), a species of major economic and conservation interest. Using third‐generation sequencing, we were able to directly detect various modification types (e.g., cytosine and adenosine methylation in all contexts) across the whole genome using amplification‐free nanopore sequencing. However, aging sites were only present in the mitogenome, which could be a specific feature of eDNA methylation or the consequence of better DNA protection within mitochondria. By considering qualitative and quantitative information about aging sites according to an objective model selection framework, our epigenetic clock reached a cross‐validated accuracy of 2.6 days (Median Absolute Error). Such performances are higher than those of previous clocks, notably for adult seabass even when scaling MAE to the age range, which could be linked to a more dynamic epigenome during early life stages. Overall, our pilot study proposes new methods to determine the potential of eDNA for simultaneous age and biodiversity assessments, although robust validation of our preliminary results along with methodological developments are needed before field applications can be envisaged.https://doi.org/10.1002/ece3.70645age estimationenvironmental DNAepigenetic clockfish larvaemethylationnanopore sequencing
spellingShingle Eliot Ruiz
Fabien Leprieur
Gérard Sposito
Martina Lüthi
Michel Schmidlin
Jacques Panfili
Loïc Pellissier
Camille Albouy
Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
Ecology and Evolution
age estimation
environmental DNA
epigenetic clock
fish larvae
methylation
nanopore sequencing
title Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
title_full Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
title_fullStr Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
title_full_unstemmed Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
title_short Environmental DNA Epigenetics Accurately Predicts the Age of Cultured Fish Larvae
title_sort environmental dna epigenetics accurately predicts the age of cultured fish larvae
topic age estimation
environmental DNA
epigenetic clock
fish larvae
methylation
nanopore sequencing
url https://doi.org/10.1002/ece3.70645
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