Intrinsic and extrinsic factors interact during development to influence telomere length in a long‐lived reptile

Abstract

The mechanisms connecting environmental conditions to plasticity in biological aging trajectories are fundamental to understanding individual variation in functional traits and life history. Recent findings suggest that telomere biology is especially dynamic during early life stages and has long‐term consequences for subsequent reproduction and survival. However, our current understanding is mostly derived from studies investigating ecological and anthropogenic factors separately, leaving the effects of complex environmental interactions unresolved. American alligators (Alligator mississippiensis) are long‐lived apex predators that rely on incubation temperature during a discrete period during development and endocrine cues to determine sex, making them especially vulnerable to current climatic variability and exposure to anthropogenic contaminants interfering with hormone function. Here, we combine field studies with a factorial design to understand how the developmental environment, along with intrinsic biological variation contribute to persistent telomere variation. We found that exposure to a common endocrine disrupting contaminant, DDE, affects telomere length, but that the directionality is highly dependent upon incubation temperature. Variation in hatchling growth, underlies a strong clutch effect. We also assess concentrations of a panel of glucocorticoid hormones and find that contaminant exposure elicits an increase in circulating glucocorticoids. Consistent with emerging evidence linking stress and aging trajectories, GC levels also appear to trend with shorter telomere length. Thus, we add support for a mechanistic link between contaminants and glucocorticoid signalling, which interacts with ecological aspects of the developmental environment to alter telomere dynamics.

Exposure to ionizing radiation disrupts normal epigenetic aging in Japanese medaka

“…Our data and those of others [ 2 , 42 ] are consistent with studies demonstrating that biological aging, as measured by telomere length, is also more dynamic during early life [ 43 – 47 ]. In most cases, increased rates of telomere attrition are associated with faster growth early in life and are thought to reflect trade-offs between growth and longevity [ 48 – 50 ]. Whereas positive correlations between accelerated epigenetic aging and individual variation in body size have been reported in humans [ 51 ], these linkages have not been explored in the context of variable life history strategies present in other ecological systems [ 12 ].…”

Genome-wide DNA methylation patterns harbor signatures of hatchling sex and past incubation temperature in a species with environmental sex determination

“…The utility of these DNAm marks as a conservation tool depends on validation using more targeted approaches (e.g., bisulfite sequencing PCR) across many samples originating from multiple geographic sites. Further, a quantitative comparison of the reliability and cost-efficiency of different potential molecular markers of sex (e.g., blood DNAm patterns, sex-biased protein levels (Tezak et al, 2020), high-sensitivity steroid hormone quantitation (Bae et al, 2021)) in TSD species is warranted.…”

“…To remove RNAlater from the preserved cells, 500 μl of phosphate-buffered saline (PBS) was added to a 200 μl aliquot of each sample and samples were centrifuged at 5000 rcf for 15 minutes at 4°C (and for an additional 5 min if a cell pellet did not form). Pelleted cells were washed once more with 500 μl of PBS and nucleic acids were isolated according to the protocol reported in (Bae et al, 2021; Appendix S1). Resulting DNA was eluted in 60 µl TE buffer (pH 8.0).…”

Editorial 2023

“…These studies show the critical impacts of stress during early‐life stages (Sheldon, Eastwood, et al, 2022; van Lieshout et al, 2022) and the presence of among‐individual variation in telomeric response to stress (Brown et al, 2022; Kärkkäinen, Laaksonen, et al, 2022; Reichard et al, 2022). Additional studies also emphasize that what qualifies as a stressor depends greatly on the biology of the organism (Friesen et al, 2022; Wood et al, 2022), and demonstrate there is much to be gained by examining telomere dynamics across diverse forms of life (Bae et al, 2022; Boonekamp et al, 2022; McLennan et al, 2022; Power et al, 2022; Rouan et al, 2022). The third suite of articles in this special issue addresses the idea that telomeres may mediate life history trade‐offs, examining correlations between telomere length and reproductive fitness (Heidinger et al, 2022; Kauzálová et al, 2022; Ravindran et al, 2022; Sepp et al, 2022) physical state (e.g., body mass, size: Atema et al, 2022; Le Pepke, Kvalnes, Rønning, et al, 2022), and cancer prevalence (Le Pepke & Eisenberg, 2022; Ujvari et al, 2022) in natural and experimental systems.…”