Telomere dynamics from hatching to sexual maturity and maternal effects in the “multivariate egg”

Abstract

Avian eggs contain a large number of molecules deposited by the mother that provide the embryo with energy but also potentially influence its development via the effects of maternally-derived hormones and antibodies: the avian egg is “multivariate”. Multivariate effects on offspring phenotype were evaluated in a sister study on captive zebra finches, by simultaneously manipulating maternally derived antibodies after LPS-treatment of mothers and egg-treatment using yolk testosterone injection. LPS-treatment had a positive effect on body mass growth at 30 days after hatching and immune response at sexual maturity, while egg-testosterone positively influenced immune response at fledging and courtship behaviour in sexually mature male offspring. Maternal effects are known to modulate offspring telomere length. Still, the multivariate effects of egg-derived maternal components on offspring telomere dynamics from hatching to sexual maturity are undefined. Here, using the data of the sister study completed with telomere measurements, we tested a) the effects of LPS and T treatments on telomere length (TL) from hatching to sexual maturity (day 82), b) how LPS treatment modulated telomere length over reproduction in adult females, and c) the relationship between maternal and offspring TL. We predicted, a) TL would be shorter in LPS fledglings (as a cost of faster growth), and b) TL would be longer in sexually mature adults from T-treated (as a proxy of individual quality). In adult females, there was an overall negative relationship between laying and rearing investments and telomere length, this relationship being weaker in LPS treated females. In chicks, there was an overall negative effect of LPS treatment on telomere length measured at fledging and sexual maturity (day 25 – 82). In addition, at fledging, there was a sex x LPS x T-treatment interaction, suggesting the existence of antagonistic effects of our treatments. Our data partially support the hypothesis of telomeres are proxies of individual quality and that individual differences in telomere length are set-up very early in life.

Genetic architecture and heritability of early‐life telomere length in a wild passerine

“…Such an association with fitness was found by Heidinger et al (2021), where early‐life TL was positively related to lifetime reproductive success in house sparrows, but only in females. Maternal effects on offspring TL are expected to be strongest in early‐life (Wolf et al, 1998) and could act through for example, yolk‐deposited components in the egg (Criscuolo et al, 2020; Noguera et al, 2020; Stier, Hsu, et al, 2020) or post‐laying through maternal care behaviour (e.g., incubation and feeding rate, Stier et al, 2020; Viblanc et al, 2020). Our results suggest that such effects may have a genetic basis that will respond to selection: For heritable traits like TL, maternal inheritance of offspring TL may be expected to increase the expected rate of adaptive evolution of TL above what would be expected from the heritability alone (Hadfield, 2012; Lande & Kirkpatrick, 1990; Räsänen & Kruuk, 2007; Wolf et al, 1998).…”

Genetic architecture and heritability of early-life telomere length in a wild passerine

“…Maternal effects on offspring TL are expected to be strongest in early-life (Wolf, Brodie Iii, Cheverud, Moore, & Wade, 1998) and could act through e.g. yolk-deposited components in the egg (Criscuolo, Torres, Zahn, & Williams, 2020;Stier et al, 2020a) or post-laying through maternal care behavior (e.g., incubation and feeding rate, Stier, Metcalfe, & Monaghan, 2020b;Viblanc et al, 2020). Since TL is a heritable trait, a positive maternal effect on offspring TL may be expected to increase the expected rate of adaptive evolution of TL (Wolf et al, 1998;Rasanen & Kruuk, 2007).…”

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

“…The prenatal hormonal environment, such as exposure to elevated glucocorticoid levels, has been coined as an important factor influencing early-life telomere length and its associated long-term outcomes (Criscuolo et al, 2020;Haussmann et al, 2012;Marchetto et al, 2016;Parolini et al, 2019). While there has been a considerable interest in prenatal glucocorticoids (Haussmann et al 2012;Tissier, Williams, and Criscuolo 2014;Noguera, da Silva, and Velando 2020) and to a lesser extent androgens (Parolini et al, 2019;Tissier et al, 2014) in the context of the 'fetal programming of telomere biology' hypothesis (Entringer et al, 2018), the potential impact of prenatal thyroid hormones has been mostly ignored so far .…”

“…Telomere length is considered as a hallmark of ageing (López-Otín et al, 2013) since telomeres shorten with age, and shorter telomeres are often predictive of lower survival or lifespan in both epidemiological and experimental studies (Arbeev et al, 2020; Heidinger et al, 2012; Muñoz-Lorente et al, 2019; Wilbourn et al, 2018). The prenatal hormonal environment, such as exposure to elevated glucocorticoid levels, has been coined as an important factor influencing early-life telomere length and its associated long-term outcomes (Criscuolo et al, 2020; Haussmann et al, 2012; Marchetto et al, 2016; Parolini et al, 2019). While there has been a considerable interest in prenatal glucocorticoids (Haussmann et al 2012; Tissier, Williams, and Criscuolo 2014; Noguera, da Silva, and Velando 2020) and to a lesser extent androgens (Parolini et al, 2019; Tissier et al, 2014) in the context of the ‘fetal programming of telomere biology’ hypothesis (Entringer et al, 2018), the potential impact of prenatal thyroid hormones has been mostly ignored so far (Stier et al 2020).…”