An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

Katharina J. Peters; Livia Gerber; Luca Scheu; Riccardo Cicciarella; Joseph A. Zoller; Zhe Fei; Steve Horvath; Simon J. Allen; Stephanie L. King; Richard C. Connor; Lee Ann Rollins; Michael Krützen

doi:10.1111/eva.13516

An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

Katharina J. Peters^*, Livia Gerber, Luca Scheu, Riccardo Cicciarella, Joseph A. Zoller, Zhe Fei, Steve Horvath, Simon J. Allen, Stephanie L. King, Richard C. Connor, Lee Ann Rollins, Michael Krützen

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

11 Citations (Scopus)

Abstract

Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These ‘epigenetic clocks’ present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.

Original language	English
Pages (from-to)	126-133
Number of pages	8
Journal	Evolutionary Applications
Volume	16
Issue number	1
Early online date	15 Dec 2022
DOIs	https://doi.org/10.1111/eva.13516
Publication status	Published - Jan 2023

Bibliographical note

Funding Information:
Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Zürich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation (P2ZHP3_200011).

Funding Information:
Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Zürich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation ( P2ZHP3_200011 ).

Publisher Copyright:
© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

Keywords

aging
bottlenose dolphin
epigenetic clock

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title = "An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus)",

abstract = "Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These {\textquoteleft}epigenetic clocks{\textquoteright} present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.",

keywords = "aging, bottlenose dolphin, epigenetic clock",

author = "Peters, {Katharina J.} and Livia Gerber and Luca Scheu and Riccardo Cicciarella and Zoller, {Joseph A.} and Zhe Fei and Steve Horvath and Allen, {Simon J.} and King, {Stephanie L.} and Connor, {Richard C.} and Rollins, {Lee Ann} and Michael Kr{\"u}tzen",

note = "Funding Information: Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Z{\"u}rich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation (P2ZHP3_200011). Funding Information: Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Z{\"u}rich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation ( P2ZHP3_200011 ). Publisher Copyright: {\textcopyright} 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.",

year = "2023",

month = jan,

doi = "10.1111/eva.13516",

language = "English",

volume = "16",

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AU - Connor, Richard C.

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N1 - Funding Information: Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Zürich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation (P2ZHP3_200011). Funding Information: Data collection for this research was carried out on Gutharraguda, Malgana Sea Country, and we acknowledge the traditional owners of the region. We thank all volunteers, RAC Monkey Mia Dolphin Resort, Monkey Mia Wildsights, and the local Department of Biodiversity, Conservation and Attractions (DBCA) staff for their continued support and assistance. Permits for the scientific use of animals were obtained from the DBCA, Western Australia. The study was carried out in compliance with the animal ethics policies of the University of Zürich, University of Bristol, and University of Western Australia. KJP was supported by a Postdoc Grant from the University of Zurich. LG was supported by an Early Postdoc Mobility Grant from the Swiss National Science Foundation ( P2ZHP3_200011 ). Publisher Copyright: © 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

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N2 - Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These ‘epigenetic clocks’ present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.

AB - Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These ‘epigenetic clocks’ present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.

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An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

Abstract

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Keywords

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