Ageing before birth: pace and stability of prenatal growth affect telomere dynamics

Abstract

Pre-natal effects on telomere length are increasingly recognized as a potential contributor to the developmental origin of health and adult diseases. While it is becoming clear that telomere length is strongly influenced by pre-natal conditions, the factors affecting telomere dynamics during embryogenesis remain poorly understood. We manipulated both the pace and stability of prenatal growth using incubation temperature in Japanese quail and investigated the impact on telomere dynamics from embryogenesis to adulthood, along with potential drivers of telomere shortening such as oxidative damage and prenatal glucocorticoid levels. Telomere length was not affected by these manipulations for the first 75% of prenatal development, but was reduced at hatching in response to both experimentally induced fast embryo growth and growth instability. These early-life effects on 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 prenatal growth appear as key factors determining telomere length and dynamics up to adulthood, with fast and unstable embryo growth leading to short telomeres with the potential for adverse associated outcomes in terms of reduced longevity and greater risk of disease.

Testing the short-and long-term effects of elevated prenatal exposure to different forms of thyroid hormones

“…40% in Okuliarová, Škrobánek & Zeman (2007) ; ca. 60% in Pick et al (2016) and in Stier, Metcalfe & Monaghan (2019) ). In addition, the injection procedure itself is also known to reduce hatching success to some extent ( Groothuis & Von Engelhardt, 2005 ).…”

Foster rather than biological parental telomere length predicts offspring survival and telomere length in king penguins

“…A large number of nonexclusive mechanisms can account for interindividual variability in telomere length early in life. In birds, for instance, telomere length may vary according to embryo exposure to maternal corticosterone in the egg (Haussmann, Longenecker, Marchetto, Juliano, & Bowden, 2012), incubation temperature (Stier, Metcalfe, & Monaghan, 2019) and/or variation in posthatching environmental conditions (Nettle et al., 2015; Reichert et al., 2015; Soler et al., 2017). Those posthatching factors include the quality of parental care and/or parental effort (as suggested by positive links between parental telomere length and breeding performance; Le Vaillant et al., 2015; Angelier et al, 2019, but see Bauch et al., 2013; Young, Barger, Dorresteijn, Haussmann, & Kitaysky, 2016).…”

The influence of phylogeny and life history on telomere lengths and telomere rate of change among bird species: A meta‐analysis

“…Prolonged incubation might also be associated with the maintenance of high telomerase activity throughout life in procellariiform species (Haussmann et al., 2004 ). An alternative explanation could be that the Hydrobatidae , which are cavity nesters where chicks grow in a very contained and stable environment, even after hatching, may exhibit metabolism that favors the maintenance of the lengths of the telomeres (Stier et al., 2019 ). This pattern supports the antagonistic pleiotropy of telomere length processes, the main hypothesis proposed to explain why species in different phylogenetic clades have evolved large differences in telomere lengths (Hemann & Greider, 2000 ).…”