Pace and stability of embryonic development affect telomere dynamics: an experimental study in a precocial bird model

Abstract

Prenatal effects on telomere length are increasingly recognized as a potential contributor to the developmental origin of health and adult disease. While it is becoming clear that telomere length is influenced by prenatal conditions, the factors affecting telomere dynamics during embryogenesis remain poorly understood. We manipulated both the pace and stability of embryonic development through varying incubation temperature and its stability in Japanese quail. We investigated the impact on telomere dynamics from embryogenesis to adulthood, together with three potential drivers of telomere shortening, growth rate, oxidative damage and prenatal glucocorticoid levels. Telomere length was not affected by our prenatal manipulation for the first 75% of embryogenesis, but was reduced at hatching in groups experiencing faster (i.e. high temperature) or less stable embryonic development. These early life differences in telomere length persisted until adulthood. The effect of developmental instability on telomere length at hatching was potentially mediated by an increased secretion of glucocorticoid hormones during development. Both the pace and the stability of embryo development appear to be key factors determining telomere length and dynamics into adulthood, with fast and less stable development leading to shorter telomeres, with the potential for adverse associated outcomes in terms of reduced longevity.

Associations between DNA methylation and telomere length during early life: insight from wild zebra finches (Taeniopygia guttata)

“…Contrary to other studies (Stier et al, 2020;Fitzpatrick et al, 2019), we did not find an effect of ambient temperature on telomere length or telomere length changes across development. Temperature has been shown to effect within individual changes in DNAm (Sheldon et al, 2020) and telomere length (Stier et al 2020;Fitzpatrick et al 2019) however, it is unclear if temperature effects these DNA modifications comparably.…”

“…DNAm and telomere length are highly responsive to environmental cues (Feil & Fraga, 2012;Monaghan, 2014), particularly during early life (Watson, Bolton & Monaghan, 2019;Boonekamp et al, 2014). For example, studies have detected associations between DNAm or telomere length and clutch/brood size (Noguera & Velando, 2020;Jimeno, Hau, Gomez-Diaz, & Verhulst, 2019;Sheldon, Schrey, Ragsdale & Griffith 2018;Nettle et al, 2016;Reichert et al, 2014;Costanzo et al, 2016;Boonekamp et al, 2014); ambient temperature (Stier, Metcalfe & Monaghan, 2020;Sheldon, Schrey, Hurley, & Griffith, 2020;Yan et al, 2015); and body size/growth rate (Young et al, 2017;Vedder et al, 2018). It is therefore important to account for these influences when testing the association between DNAm and telomere length.…”

Does parental heart rate affect embryonic heart rate during incubation? An experiment in Common Terns Sterna hirundo

“…Other studies have suggested that embryonic heart rate in birds is sensitive to environmental conditions (Sheldon et al 2018), in particular to temperature (Vedder et al 2017;Sheldon et al 2018;Stier et al 2020). Indeed, we found a decrease in embryonic heart rate as egg temperature declined during the measurement at room temperature (see Table 1a).…”

Born to be young? Prenatal thyroid hormones increase early-life telomere length in wild collared flycatchers

“…It was unfortunately not possible to evaluate any long-lasting impact of prenatal THs supplementation on adult telomere length. Yet, considering that most telomere dynamics occurs during the growth period and that telomere length is a repeatable trait [13,14], it is likely that the effects of prenatal THs observed here on early-life telomere length would be carried over the adult stage. The positive effect of prenatal THs on telomere length is unlikely related to oxidative stress prevention, since we previously found no differences in oxidative stress markers in these experimental birds [6], or in a similar experiment in a closely-related species [22].…”

“…There is evidence that telomere length could reflect phenotypic quality since early-life telomere length has been shown for instance to predict lifespan [11] and fitness [12] in avian species. Interestingly, a large part of the inter-individual F o r R e v i e w O n l y variation in telomere length could already be set at birth, and thus may be partially caused by different exposure to maternal hormones [13,14].…”