Multi-Tissue Methylation Clocks for Age and Sex Estimation in the Common Bottlenose Dolphin

Robeck, Todd R.; Fei, Zhe; Haghani, Amin; Zoller, Joseph A.; Li, Caesar Z.; Steinman, Karen J.; DiRocco, Stacy; Staggs, Lydia; Schmitt, Todd L.; Osborn, S. B.; Montano, Gisele A.; Rodríguez, Magdalena; Horvath, Steve

doi:10.3389/fmars.2021.713373

Cited by 11 publications

(18 citation statements)

References 72 publications

(73 reference statements)

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“…The previously published species‐specific clock for common bottlenose dolphins (Robeck, Fei, Haghani, et al, 2021 ) based on skin samples, and the clock based on skin and blood samples, predicted age for our samples with an accuracy of r = 0.83 and r = 0.75, and MAE = 0.22 and MAE = 9.6, respectively. The multi‐species odontocete clock for skin samples and for skin and blood samples (Robeck, Fei, Lu, et al, 2021 ) predicted age for our samples with an accuracy of r = 0.68 and r = 0.76, and MAE = 6.8 and MAE = 3.5 years, respectively (Figure 1 ).…”

Section: Resultsmentioning

confidence: 54%

“… Epigenetic ages calculated using elastic net regression models with leave‐one‐out‐cross‐validation applied to 68 skin samples of Indo‐Pacific bottlenose dolphins ( Tursiops aduncus ) for which age was known with an accuracy of ±1 year. Ages were calculated using (a) the species‐specific clock developed in this study, (b) the skin clock developed for Tursiops truncatus (Robeck, Fei, Haghani, et al, 2021 ), (c) the skin and blood clock developed for T. truncatus (Robeck, Fei, Haghani, et al, 2021 ), (d) the skin clock for multi‐species odontocetes (Robeck, Fei, Lu, et al, 2021 ), and (e) the skin and blood clock for multi‐species odontocetes (Robeck, Fei, Lu, et al, 2021 ). Regression lines are shown in blue ( T. aduncus clock), orange ( T. truncatus clocks) and red (multi‐species odontocete clocks), dotted diagonal indicates a perfect correlation ( y = x ), and points represent individual animals.…”

Section: Resultsmentioning

confidence: 99%

“…To assess our clock's performance in relation to that of other epigenetic clocks, we subsequently compared our species‐specific epigenetic clocks with the previously published species‐specific common bottlenose dolphin clock (Robeck, Fei, Haghani, et al, 2021 ) and the multi‐species Odontocete Epigenetic Aging Clock (OEAC; Robeck, Fei, Lu, et al, 2021 ) for skin tissues as well as for skin and blood. For this, we applied these four clocks to our samples of known age and compared their respective r values with that of our species‐specific clocks for Indo‐Pacific bottlenose dolphins.…”

Section: Methodsmentioning

confidence: 99%

“…Multi‐species clocks effectively estimate age and sex of individual members of various species simultaneously and, thus, facilitate conservation efforts by enabling the investigation of population viability of multiple species with a single tool (Robeck, Fei, Lu, et al, 2021 ). Nevertheless, accuracy of age predictions can be improved with species‐specific clocks (Field et al, 2018 ; Zhang et al, 2019 ), several of which currently exist for odontocetes, including belugas (Bors et al, 2021 ) and common bottlenose dolphins (Barratclough et al, 2021 ; Beal et al, 2019 ; Robeck, Fei, Haghani, et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

“…Here, we present a species‐specific age estimation clock as well as sex predictor based on DNA methylation data extracted from skin samples of Shark Bay's Indo‐Pacific bottlenose dolphin population. We further compare the accuracy of age estimates from this clock for our data with that of the multi‐species odontocete clock (Robeck, Fei, Lu, et al, 2021 ) and the common bottlenose dolphin clock (Robeck, Fei, Haghani, et al, 2021 ). Our epigenetic clock will inform species conservation management, as well as studies focusing on population biology, social organisation and behavior, throughout their broad range.…”

Section: Introductionmentioning

confidence: 99%

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

Peters

Gerber

Scheu

et al. 2022

Evolutionary Applications

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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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Section: Resultsmentioning

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Peters

Gerber

Scheu

et al. 2022

Evolutionary Applications

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Using epigenetic clocks to investigate changes in the age structure of critically endangered Māui dolphins

Hernandez,

O'Neill,

Bors

et al. 2023

Ecology and Evolution

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The age of an individual is an essential demographic parameter but is difficult to estimate without long‐term monitoring or invasive sampling. Epigenetic approaches are increasingly used to age organisms, including nonmodel organisms such as cetaceans. Māui dolphins (Cephalorhynchus hectori maui) are a critically endangered subspecies endemic to Aotearoa New Zealand, and the age structure of this population is important for informing conservation. Here we present an epigenetic clock for aging Māui and Hector's dolphins (C. h. hectori) developed from methylation data using DNA from tooth aged individuals (n = 48). Based on this training data set, the optimal model required only eight methylation sites, provided an age correlation of .95, and had a median absolute age error of 1.54 years. A leave‐one‐out cross‐validation analysis with the same parameters resulted in an age correlation of .87 and median absolute age error of 2.09 years. To improve age estimation, we included previously published beluga whale (Delphinapterus leucas) data to develop a joint beluga/dolphin clock, resulting in a clock with comparable performance and improved estimation of older individuals. Application of the models to DNA from skin biopsy samples of living Māui dolphins revealed a shift from a median age of 8–9 years to a younger population aged 7–8 years 10 years later. These models could be applied to other dolphin species and demonstrate the ability to construct a clock even when the number of known age samples is limited, removing this impediment to estimating demographic parameters vital to the conservation of critically endangered species.

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Pan-primate studies of age and sex

Horvath

Haghani²,

Zoller

et al. 2023

GeroScience

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Age and sex have a profound effect on cytosine methylation levels in humans and many other species. Here we analyzed DNA methylation profiles of 2400 tissues derived from 37 primate species including 11 haplorhine species (baboons, marmosets, vervets, rhesus macaque, chimpanzees, gorillas, orangutan, humans) and 26 strepsirrhine species (suborders Lemuriformes and Lorisiformes). From these we present here, pan-primate epigenetic clocks which are highly accurate for all primates including humans (age correlation R = 0.98). We also carried out in-depth analysis of baboon DNA methylation profiles and generated five epigenetic clocks for baboons (Olive-yellow baboon hybrid), one of which, the pan-tissue epigenetic clock, was trained on seven tissue types (fetal cerebral cortex, adult cerebral cortex, cerebellum, adipose, heart, liver, and skeletal muscle) with ages ranging from late fetal life to 22.8 years of age. Using the primate data, we characterize the effect of age and sex on individual cytosines in highly conserved regions. We identify 11 sex-related CpGs on autosomes near genes (POU3F2, CDYL, MYCL, FBXL4, ZC3H10, ZXDC, RRAS, FAM217A, RBM39, GRIA2, UHRF2). Low overlap can be observed between age- and sex-related CpGs. Overall, this study advances our understanding of conserved age- and sex-related epigenetic changes in primates, and provides biomarkers of aging for all primates.

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Multi-Tissue Methylation Clocks for Age and Sex Estimation in the Common Bottlenose Dolphin

Cited by 11 publications

References 72 publications

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

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

Using epigenetic clocks to investigate changes in the age structure of critically endangered Māui dolphins

Pan-primate studies of age and sex

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