Altricial bird early-stage embryos express the molecular ‘machinery’ to respond to maternal thyroid hormone cues

Abstract

Maternal hormones, such as thyroid hormones transferred to embryos and eggs, are key signalling pathways to mediate maternal effects. To be able to respond to maternal cues, embryos must express key molecular "machinery" of the hormone pathways, such as enzymes and receptors. While altricial birds begin thyroid hormone (TH) production only at/after hatching, experimental evidence suggests that their phenotype can be influenced by maternal THs deposited in the egg. However, it is not understood, how and when altricial birds express genes in the TH-pathway. For the first time, we measured the expression of key TH-pathway genes in altricial embryos, using two common altricial ecological model species (pied flycatcher, Ficedula hypoleuca and blue tit Cyanistes caeruleus). Deiodinase DIO1 gene expression could not be reliably confirmed in either species, but deiodinase enzyme DIO2 and DIO3 genes were expressed in both species. Given that DIO2 coverts T4 to biologically active T3, and DIO3 mostly T3 to inactive forms of thyroid hormones, our results suggest that embryos may modulate maternal signals. Thyroid hormone receptor (THRA and THRB) and monocarboxyl membrane transporter gene (SLC15A2) were also expressed, enabling TH-responses. Our results suggest that early altricial embryos may be able to respond and potentially modulate maternal signals conveyed by thyroid hormones.

Maternally transferred thyroid hormones and life‐history variation in birds

“…In oviparous animals, such as birds, maternal THs are transferred and deposited into egg yolks during egg formation, from where they can reach the embryos and influence developmental process, and eventually offspring phenotype (Ruuskanen & Hsu, 2018). Although early embryos are not yet able to produce endogenous THs, they already express necessary molecules, including TH receptors and deiodinases, to respond to maternal THs in less than 4 days of incubation (Flamant & Samarut, 1998; van Herck et al, 2012, 2015; Too et al, 2017; Ruuskanen, Hukkanen, et al, 2021). Experimental manipulation of THs during early embryo development (albeit often using supraphysiological doses) has demonstrated influences on development and gene expression in chickens Gallus gallus domesticus (Flamant & Samarut, 1998; Darras et al, 2009; Darras, 2019), Japanese quail Coturnix japonica (Wilson & McNabb, 1997), frogs Xenopus tropicalis (Duarte‐Guterman et al, 2010) and various fishes (reviewed in Brown et al, 2014).…”