Effect of prenatal glucocorticoids and thyroid hormones on developmental plasticity of mitochondrial aerobic metabolism, growth and survival: an experimental test in wild great tits

Abstract

Developmental plasticity is partly mediated by transgenerational effects, including those mediated by the maternal endocrine system. Glucocorticoid and thyroid hormones may play central roles in developmental programming through their action on metabolism and growth. However, the mechanisms by which they affect growth and development remain understudied. One hypothesis is that maternal hormones directly affect the production and availability of energy-carrying molecules (e.g. ATP) by their action on mitochondrial function. To test this hypothesis, we experimentally increased glucocorticoid and thyroid hormones in wild great tit eggs (Parus major) to investigate their impact on offspring mitochondrial aerobic metabolism (measured in blood cells), and subsequent growth and survival. We show that prenatal glucocorticoid supplementation affected offspring cellular aerobic metabolism by decreasing mitochondrial density, maximal mitochondrial respiration and oxidative phosphorylation, while increasing the proportion of the maximum capacity being used under endogenous conditions. Prenatal glucocorticoid supplementation only had mild effects on offspring body mass, size and condition during the rearing period, but led to a sex-specific (females only) decrease in body mass a few months after fledging. Contrary to our expectations, thyroid hormones supplementation did not affect offspring growth or mitochondrial metabolism. Recapture probabilities as juveniles or adults were not significantly affected by prenatal hormonal treatments. Our results demonstrate that prenatal glucocorticoids can affect post-natal mitochondrial density and aerobic metabolism. The weak effects on growth and apparent survival suggest that nestlings were mostly able to compensate for the transient decrease in mitochondrial aerobic metabolism induced by prenatal glucocorticoids.

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

“…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). Yet, our measurements are limited to blood and tissue-specific effects of TH on mitochondrial density or TH-related cellular machinery (receptors and converting enzymes; Ruuskanen et al 2022) may occur as this has been shown for instance for glucocorticoids (Weber et al 2002). According to the metabolic telomere attrition hypothesis, telomere shortening is likely to be increased during energy-demanding periods, and accelerated growth under limited resources is likely carrying a metabolic cost (Casagrande and Hau, 2019).…”

Maternally transferred thyroid hormones and life‐history variation in birds

“…In experiments with a direct elevation of yolk THs in altricial pigeons and precocial quail, incubation duration was not extended (Hsu et al, 2017; Sarraude et al, 2020b). In fact, experimentally elevated yolk THs might even shorten incubation duration (in great tits, Cossin‐Sevrin et al, 2022). In a reptile species (short‐necked turtles Emydura macquarii ), exogenously injected T3 in the middle of incubation was also found to shorten incubation duration (McGlashan et al, 2017).…”

“…In experiments with a direct elevation of yolk THs in altricial pigeons and precocial quail, incubation duration was not extended (Hsu et al, 2017;Sarraude et al, 2020b). In fact, experimentally elevated yolk THs might even shorten incubation duration (in great tits, Cossin-Sevrin et al, 2022).…”

Manipulating plasma thyroid hormone levels alters development of endothermy and ventilation in nestling red-winged blackbirds

“…Thyroid hormones are important for a number of developmental processes in birds during hatching and nestling development ( De Groef et al, 2013 ). A number of recent studies examined the influence of maternal thyroid hormones passed on in the egg on subsequent development in altricial species development ( Hsu et al, 2020 ; Sarraude et al, 2020 ; Cossin-Sevrin et al, 2022 ). Elevating egg yolk thyroid hormones resulted in earlier hatching and larger hatchlings in collared flycatchers ( Ficedula albicollis ) ( Hsu et al, 2019 ) but had no effect in the great tit hatchling ( Parus major ) ( Cossin-Sevrin et al, 2022 ).…”

“…A number of recent studies examined the influence of maternal thyroid hormones passed on in the egg on subsequent development in altricial species development ( Hsu et al, 2020 ; Sarraude et al, 2020 ; Cossin-Sevrin et al, 2022 ). Elevating egg yolk thyroid hormones resulted in earlier hatching and larger hatchlings in collared flycatchers ( Ficedula albicollis ) ( Hsu et al, 2019 ) but had no effect in the great tit hatchling ( Parus major ) ( Cossin-Sevrin et al, 2022 ). The effect on the collared flycatcher disappeared quickly in the developing nestling.…”