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Accurate determination of an animal's age is a central criterion for understanding many aspects of its life, such as growth rate, age at maturity, peak reproductive performance, and life span; making age a crucial parameter to unravel key life history characteristics (Stearns, 1976). Furthermore, at the population level, large-scale demographic age and generation time information are critical for assessing population viability (Heydenrych et al., 2021; Manlik et al., 2022). However, estimating age in free-ranging animals is often difficult, particularly for long-lived, highly mobile species, such as cetaceans (whales, dolphins, and porpoises; Read et al., 2018). While age information can be reliably gained from behavioral records, this requires a long-term study effort, typically spanning multiple decades, until the entire age range of individuals in the population can be determined. Alternatively, age can be estimated via the correlation of certain morphological or molecular traits with the known age of individuals. In mammals, most morphological age estimators suffer from low accuracy or require highly invasive procedures, rendering them unfeasible for application to many individuals. Toothed whales (odontocetes), for example, are often aged approximately via their total body length, which allows only a crude estimation of life-stage (i.e., calf/juvenile/adult; Betty et al., 2022; Chivers, 2009). Another, more accurate method of aging odontocetes is via longitudinal sectioning and quantification of growth layers in their teeth. While this method is deemed relatively robust, differing levels of tooth wear depending on age and feeding techniques can confound results (Hohn & Fernandez, 1999; Perrin et al., 1980; Waugh et al., 2018). Furthermore, this method is largely restricted to deceased individuals due to its invasiveness and is, thus, logistically unfeasible for the majority of free-ranging odontocetes (but see Hohn et al., 1989). In some species, the Indo-Pacific bottlenose dolphin (Tursiops aduncus) for example, morphological traits such as skin speckling patterns can indicate age, but the approach is limited by a number of factors, including the observers' ability to image the entire body, variation between individuals in speckling rates, and differences in ‘capture’ probability across a population, and thus results are approximate at best (Krzyszczyk & Mann, 2012; Yagi et al., 2022). The idea of using telomere length as an indicator of age has received much attention in recent decades, but the decline in telomere length is weak and too variable across vertebrate classes to deliver reliable estimates (Dunshea et al., 2011; Jylhävä et al., 2017; Olsen et al., 2012). Recent advances in sequencing technology have opened new avenues for precise age determination using DNA methylation data. The resultant ‘epigenetic clocks’ are based on correlates between age and DNA methylation of specific cytosine-guanine (CpG) sites and are currently considered the best age predictors available (De PaoliIseppi et al., 2017; Guevara & Lawler, 2018; Jylhävä et al., 2017). The CpG sites used to build epigenetic clocks can also be used to reliably predict sex. This is particularly useful for species that are difficult to observe and lack clear sexual dimorphism, such as some odontocetes. Robeck, Fei, Lu, et al. (2021) built a multi-species clock to estimate age and predict sex for odontocetes, which was crossvalidated for nine species (common bottlenose dolphin T. truncatus, beluga Delphinapterus leucas, killer whale Orcinus orca, Pacific whitesided dolphin Lagenorhynchus obliquidens, short-finned pilot whales Globicephala macrorhynchus, rough-toothed dolphin Steno bredanensis, Commerson's dolphin Cephalorhynchus commersonii, common dolphin Delphinus delphis, harbour porpoise Phocoena phocoena). 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). The Shark Bay Indo-Pacific bottlenose dolphin population off Monkey Mia, Western Australia, has been studied in considerable depth since the early 1980s (Connor & Smolker, 1985), making it one of the best-known dolphin populations in the world (Allen et al., 2016; Connor & Krützen, 2015; Krützen et al., 2004). Photo-identification records and the social behavior of Shark Bay's dolphins have been documented for 40 years, so year of birth and sex are known for most individuals (Connor & Krützen, 2015; King et al., 2021). To date, when no birthdate is known, the age of dolphins could only be roughly estimated using a suite of approximate measures, such as birth of first calf (females), first herding of females for reproductive purposes (males), individual sighting histories, and skin speckling patterns (Krzyszczyk & Mann, 2012). The lack of reliable age estimates has been a limiting factor in research relating to dolphin reproduction and life history (but see Karniski et al., 2018; Taylor et al., 2007). Outside Shark Bay, Indo-Pacific bottlenose dolphins are widely distributed, ranging from coastal areas in the Indian Ocean throughout Southeast Asia to parts of the western Pacific (Wang, 2018). The development of epigenetic aging clocks requires samples from animals with known ages for calibration, so the Shark Bay population offers an exceptional opportunity to build a species-specific clock for Indo-Pacific bottlenose dolphins using samples collected from wild animals. 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.
- Accurate determination of animal's age
- Importance in understanding life history characteristics
- Growth rate
- Age at maturity
- Peak reproductive performance
- Life span
- Importance in assessing population viability
- Large-scale demographic age and generation time information
- Difficulties in estimating age in free-ranging animals
- Particularly long-lived, highly mobile species (cetaceans)
- Long-term study effort for behavioral records
- Correlation of morphological or molecular traits with known age
- Methods of aging odontocetes (toothed whales)
- Total body length estimation
- Longitudinal sectioning and growth layer quantification in teeth
- Confounding factors of tooth wear and feeding techniques
- Morphological traits (skin speckling patterns)
- Limitations of imaging, variation, and capture probability
- Telomere length decline
- Weak and variable across vertebrate classes
- DNA methylation data
- Epigenetic clocks based on correlates between age and DNA methylation at CpG sites
- Considered the best age predictors
- Species-specific clocks for odontocetes
- Shark Bay Indo-Pacific bottlenose dolphin population
- Well-studied population with photo-identification and social behavior records
- Lack of reliable age estimates
- Opportunity to develop a species-specific epigenetic clock using DNA methylation data from skin samples
- Species-specific age estimation clock and sex predictor for Indo-Pacific bottlenose dolphins
- Based on DNA methylation data
- Comparison with multi-species odontocete clock and common bottlenose dolphin clock
- Importance of the epigenetic clock in species conservation management and population biology studies throughout their range.
Concept Map:
Age determination in animals
- Importance of accurate age determination
- Understanding life history characteristics
- Growth rate
- Age at maturity
- Peak reproductive performance
- Life span
- Assessing population viability
- Large-scale demographic age and generation time information
Challenges in estimating age in free-ranging animals
- Difficulty in estimating age for long-lived, highly mobile species
- Cetaceans (whales, dolphins, and porpoises)
- Reliable age information from behavioral records requires long-term study effort
- Spanning multiple decades
- Alternative methods of age estimation
- Correlation of morphological or molecular traits with known age
- Most morphological age estimators suffer from low accuracy or require invasive procedures
- Toothed whales aged approximately via total body length
- More accurate method: longitudinal sectioning and quantification of growth layers in teeth
- Tooth wear and feeding techniques can confound results
- Largely restricted to deceased individuals
- Other methods of age estimation
- Skin speckling patterns
- Limitations: variability, observer ability, capture probability
- Telomere length as an indicator of age
- Weak decline with too much variability
- DNA methylation data and epigenetic clocks
- Best age predictors available
- Precise age determination using sequencing technology
- CpG sites used to build clocks can also predict sex
Species-specific age estimation clocks
- Multi-species clock for odontocetes
- Estimates age and predicts sex for multiple species simultaneously
- Facilitates conservation efforts and population viability investigation
- Accuracy can be improved with species-specific clocks
- Existing clocks for belugas and common bottlenose dolphins
Shark Bay Indo-Pacific bottlenose dolphin population
- Well-known dolphin population studied since the early 1980s
- Photo-identification records and social behavior data available
- Age estimation limitations: approximate measures, speckling patterns
- Opportunity to build a species-specific age estimation clock using samples from wild animals
Benefits of species-specific age estimation clock
- Informs species conservation management
- Supports research on population biology, social organization, and behavior
- Applicable throughout the wide range of Indo-Pacific bottlenose dolphins