Age estimation in a long‐lived seabird (Ardenna tenuirostris) using DNA methylation‐based biomarkers

Abstract

Age structure is a fundamental aspect of animal population biology. Age is strongly related to individual physiological condition, reproductive potential and mortality rate. Currently, there are no robust molecular methods for age estimation in birds. Instead, individuals must be ringed as chicks to establish known‐age populations, which is a labour‐intensive and expensive process. The estimation of chronological age using DNA methylation (DNAm) is emerging as a robust approach in mammals including humans, mice and some non‐model species. Here, we quantified DNAm in whole blood samples from a total of 71 known‐age Short‐tailed shearwaters (Ardenna tenuirostris) using digital restriction enzyme analysis of methylation (DREAM). The DREAM method measures DNAm levels at thousands of CpG dinucleotides throughout the genome. We identified seven CpG sites with DNAm levels that correlated with age. A model based on these relationships estimated age with a mean difference of 2.8 years to known age, based on validation estimates from models created by repeated sampling of training and validation data subsets. Longitudinal observation of individuals re‐sampled over 1 or 2 years generally showed an increase in estimated age (6/7 cases). For the first time, we have shown that epigenetic changes with age can be detected in a wild bird. This approach should be of broad interest to researchers studying age biomarkers in non‐model species and will allow identification of markers that can be assessed using targeted techniques for accurate age estimation in large population studies.

A clockwork fish: Age prediction using DNA methylation‐based biomarkers in the European seabass

“…For example, in humans the tick rate is high until adulthood is reached and then it slows down and remains constant (Horvath, ). In short‐tailed shearwaters, a larger variability in DNA methylation was found at younger ages, although the few samples of young birds was a limiting factor for this study (Paoli‐Iseppi et al, ). In the European sea bass, by contrast, we had a large number of juvenile individuals of less than 1.5 years.…”

The Bottlenose Dolphin Epigenetic Aging Tool (BEAT): A Molecular Age Estimation Tool for Small Cetaceans

“…This modification is found at 60-80% of CpG sites (where a cytosine, C, is next to a guanine, G, in the DNA sequence) across vertebrate genomes (Jones, 2001(Jones, , 2012 both at gene bodies and promoters (Deaton and Bird, 2011), participating in the regulation of gene expression in response to developmental and environmental signals (Eirin-Lopez and Putnam, 2018). Most importantly, it has been shown that the %DNA methylation at specific positions of certain genes correlates linearly with chronological age, making age prediction reliable as demonstrated in the case of mammals including humans (Grönniger et al, 2010;Polanowski et al, 2014), as well as in other vertebrates (Paoli-Iseppi et al, 2019). This property has boosted the development of epigenetic aging tools that are now being successfully used in human forensics (Horvath, 2013;Shabani et al, 2018) as well as in marine organisms (Polanowski et al, 2014;Eirin-Lopez and Putnam, 2018).…”

Demographic, Spatial, and Epigenetic Response of the Louisiana Waterthrush (Parkesia Motacilla) to Shale Gas Development

“…Our study is the second for a wild bird population that suggests methylation varies with age. Humans have an epigenetic clock where methylation increases with age (Horvath 2013), but waterthrush generally displayed decreased methylation with age, similar to that found in a seabird at most age-related restriction sites (De Paoli-Iseppi et al 2018). In addition to methylation varying with pollutant concentrations as previously seen in a wild bird population (Romano et al 2016), our study is the first for a wild bird population to suggest a potential sex-specific epigenetic response to contaminants.…”

“…5b) I hypothesized older adults to have fewer methylated restriction sites than younger adults because decreased methylation is correlated with age in birds (De Paoli-Iseppi et al 2019). Similarly, I expected nestlings to be differentially methylated from adults.…”