Testing for context-dependent effects of prenatal thyroid hormones on offspring survival and physiology: an experimental temperature manipulation

Hsu, Bin-Yan; Sarraude, Tom; Cossin-Sevrin, Nina; Crombecque, Melanie; Stier, Antoine; Ruuskanen, Suvi

doi:10.1038/s41598-020-71511-y

Cited by 12 publications

(23 citation statements)

References 56 publications

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“…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]. The selective disappearance of THembryos with short telomeres could potentially explain why chicks hatched from TH-eggs have longer telomeres than controls.…”

Section: Resultsmentioning

confidence: 66%

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

et al. 2020

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The underlying mechanisms of the lifelong consequences of prenatal environmental condition on health and ageing remain little understood. Thyroid hormones (THs) are important regulators of embryogenesis, transferred from the mother to the embryo. Since prenatal THs can accelerate early-life development, we hypothesized that this might occur at the expense of resource allocation in somatic maintenance processes, leading to premature ageing. Therefore, we investigated the consequences of prenatal TH supplementation on potential hallmarks of ageing in a free-living avian model in which we previously demonstrated that experimentally elevated prenatal TH exposure accelerates early-life growth. Using cross-sectional sampling, we first report that mitochondrial DNA (mtDNA) copy number and telomere length significantly decrease from early-life to late adulthood, thus suggesting that these two molecular markers could be hallmarks of ageing in our wild bird model. Elevated prenatal THs had no effect on mtDNA copy number but counterintuitively increased telomere length both soon after birth and at the end of the growth period (equivalent to offsetting ca 4 years of post-growth telomere shortening). These findings suggest that prenatal THs might have a role in setting the ‘biological' age at birth, but raise questions about the nature of the evolutionary costs of prenatal exposure to high TH levels.

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Section: Resultsmentioning

confidence: 66%

“…Such potential context-dependent effects will require experimental manipulations of both egg THs and environmental conditions in order to be revealed (e.g. [22]). royalsocietypublishing.org/journal/rsbl Biol.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2020

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“…was not supported as we found no evidence for differences in mitochondrial density or plasma TH levels (key coordinators of metabolism) across the treatment groups. The latter results are not fully surprising considering the limited evidence supporting a prenatal programming of plasma THs (sex-specific effect on T4 only, Hsu et al 2017;no effect, Hsu et al 2020) or mitochondrial density (no effect, Hsu et al 2020). According to the metabolic telomere attrition hypothesis, telomere shortening is likely to be increased during energydemanding periods, and accelerated growth under limited resources is likely carrying a metabolic cost (Casagrande and Hau, 2019).…”

Section: Discussionmentioning

confidence: 95%

“…Variation in exposure to prenatal thyroid hormones (T3, triiodothyronine, and T4, thyroxine) could influence telomere length via several mutually non-exclusive proximate pathways: (i) Prenatal THs can stimulate growth (yet results are inconsistent across studies and species, (Hsu et al, 2020(Hsu et al, , 2019a(Hsu et al, , 2017Medici et al, 2013;Ruuskanen et al, 2016a;Sarraude et al, 2020a;Sarraude et al, 2020b;Vrijkotte et al, 2017;Zhang et al, 2019), which can directly contribute to telomere attrition through increasing cellular division (Monaghan and Ozanne, 2018;, or indirectly accelerate telomere shortening through increasing oxidative stress (Monaghan and Ozanne, 2018;Reichert and Stier, 2017;Smith et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Prenatal thyroid hormones accelerate postnatal growth and telomere shortening in wild great tits

Hsu

Cossin-Sevrin

Stier

et al. 2021

Preprint

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Early-life environment is known to affect later-life health and disease, which could be mediated by the early-life programming of telomere length, a key hallmark of ageing. According to the fetal programming of telomere biology hypothesis, variation in prenatal exposure to hormones is likely to influence telomere length. Yet the contribution of key metabolic hormones, i.e. thyroid hormones (THs), has been largely ignored. We recently showed that in contrast to predictions, exposure to elevated prenatal THs increased postnatal telomere length in wild collared flycatchers, but the generality of such effect, its underlying proximate mechanisms and consequences on survival have not been investigated. We therefore conducted a comprehensive study evaluating the impact of THs on potential drivers of telomere dynamics (growth, post-natal THs, mitochondria and oxidative stress), telomere length and medium-term survival using wild great tits as a model system. While prenatal THs did not significantly affect telomere length after hatching (i.e. day 7), they influenced postnatal telomere shortening (i.e. shorter telomeres at day 14 and the following winter) but not apparent survival. Circulating THs, mitochondrial density or oxidative stress biomarkers were not significantly influenced, whereas TH-supplemented group showed accelerated growth, which may explain the observed delayed effect on telomeres. We discuss several alternative hypotheses that may explain the contrast with our previous findings in flycatchers. Given that shorter telomeres in early life tend to be carried until adulthood and are often associated with decreased survival prospects, the effects of prenatal THs on telomeres may have long-lasting effects on senescence.

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“…More specifically, T 4 levels were negatively correlated with ambient temperature in great tits Parus major (Ruuskanen et al, 2016). However, in wild pied flycatchers Ficedula hypoleuca, there is no evidence for context-dependent effects of prenatal TH related to postnatal temperature on growth, survival, and plasma TH levels (Hsu et al, 2020), suggesting species differences or unknown confounding effects.…”

Section: Climate Changes and Terrestrial Biodiversitymentioning

confidence: 94%

Interdependence of Thyroid and Corticosteroid Signaling in Vertebrate Developmental Transitions

2021

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Post-embryonic acute developmental processes mainly allow the transition from one life stage in a specific ecological niche to the next life stage in a different ecological niche. Metamorphosis, an emblematic type of these post-embryonic developmental processes, has occurred repeatedly and independently in various phylogenetic groups throughout metazoan evolution, such as in cnidarian, insects, molluscs, tunicates, or vertebrates. This review will focus on metamorphoses and developmental transitions in vertebrates, including typical larval metamorphosis in anuran amphibians, larval and secondary metamorphoses in teleost fishes, egg hatching in sauropsids and birth in mammals. Two neuroendocrine axes, the hypothalamic-pituitary-thyroid and the hypothalamic-pituitary-adrenal/interrenal axes, are central players in the regulation of these life transitions. The review will address the molecular and functional evolution of these axes and their interactions. Mechanisms of integration of internal and environmental cues, and activation of these neuroendocrine axes represent key questions in an “eco-evo-devo” perspective of metamorphosis. The roles played by developmental transitions in the innovation, adaptation, and plasticity of life cycles throughout vertebrates will be discussed. In the current context of global climate change and habitat destruction, the review will also address the impact of environmental factors, such as global warming and endocrine disruptors on hypothalamic-pituitary-thyroid and hypothalamic-pituitary-adrenal/interrenal axes, and regulation of developmental transitions.

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Testing for context-dependent effects of prenatal thyroid hormones on offspring survival and physiology: an experimental temperature manipulation

Cited by 12 publications

References 56 publications

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

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

Prenatal thyroid hormones accelerate postnatal growth and telomere shortening in wild great tits

Interdependence of Thyroid and Corticosteroid Signaling in Vertebrate Developmental Transitions

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