Maternal Thyroid Hormones: An Unexplored Mechanism Underlying Maternal Effects in an Ecological Framework

Abstract

Maternal effects are currently acknowledged as important causes of transgenerational phenotypic variation and a potential mechanism to adapt offspring to predicted environments, thus having a pivotal role in ecology and evolution. Research in hormonal mechanism underlying maternal effects has focused heavily on steroid hormones. Other hormones, such as thyroid hormones (THs; thyroxine and triiodothyronine), have been largely ignored in ecological research until recently. We summarize the recent findings, identify knowledge gaps, and provide future research directions investigating the role of TH-mediated maternal effects in ecological context across taxa. Surprisingly, data on the sources of naturally occurring variation in maternal THs and their fitness effects are lacking in most vertebrate taxa. There is considerable variation in maternal TH levels in eggs across taxa. Avian egg THs show heritable variation, and data from fish and amphibians suggest female consistency in egg TH levels. In birds, variation in maternal THs was associated with important ecological factors, such as food availability and temperature. THs also showed intraindividual variation varying systematically within clutches. Importantly, exposure to maternal THs within naturally occurring range affected offspring fitness-related traits (growth and survival) in birds and fish. These findings make THs an interesting mechanism underlying maternal effects, which likely shape offspring phenotypes.

Acute stressors experienced by layer breeders do not affect measures of stress and fear in their offspring

“…Previous studies have shown strong effects on metabolic and developmental processes (6,8,17), but the extent to which corticosterone affects the behaviour of the offspring remains unclear and appears to depend on delivery method and species (18). More recently, other biological components in the egg, such thyroid hormones (19,20), antioxidants (21), immunoglobulins (22), and especially androgens (23) have also been suggested as potential mediators of maternal stress in poultry species.…”

Elevated exposure to prenatal thyroid hormones affects embryonic mortality but has no clear effects into adulthood

“…Historically, research on maternal hormones has mostly focused 46 on steroid hormones von Engelhardt and Groothuis, 2011). Recently,47 thyroid hormones (THs) also received attention in the context of hormone-mediated maternal 48 effects (Ruuskanen and Hsu, 2018). 49…”

Prenatal thyroid hormone exposure increases growth but not oxidative stress in a wild passerine species

“…Most studies in the field of hormone-mediated maternal effects have focussed on 45 steroid hormones, especially cortisol, corticosterone and androgens (von Engelhardt and 46 Groothuis, 2011). However, mothers transfer other hormones to their embryo (Williams and 47 Groothuis, 2015), including thyroid hormones (Ruuskanen and Hsu, 2018) that deserve much 48 more attention. 49…”

“…Thyroid hormones (THs) are metabolic hormones produced by the thyroid gland and 50 are present in two main forms: the prohormone thyroxine (T 4 ) and the biologically active 51 form triiodothyronine (T 3 ). Thyroid hormones have pleiotropic effects that serve several 52 biologically important functions across vertebrates (Ruuskanen and Hsu, 2018). In early-life, 53 they participate in the maturation of multiple tissues (e.g., birds, McNabb and Darras, 2015;54 mammals, Pascual and Aranda, 2013), and interact with growth hormones to increase growth 55 (McNabb and Darras, 2015).…”

“…Together with their relatively 79 well-known ecology and evolution, birds have become the most extensively studied taxa in 80 research on the function of maternal hormones (Groothuis and Schwabl, 2008;von Engelhardt 81 and Groothuis, 2011). 82 Maternal thyroid hormones have long been detected in egg yolks of chicken (Hilfer 83 and Searls, 1980;Prati et al, 1992) and Japanese quail (Wilson and McNabb, 1997), although 84 these hormones have received very little attention (Ruuskanen and Hsu, 2018). To date, only 85 three studies have investigated the effects of physiological variations in yolk THs on offspring 86 development (great tits, Parus major, Ruuskanen et al, 2016;rock pigeons, Columba livia, 87 Hsu et al, 2017;collared flycatchers, Ficedula albicollis, Hsu et al, 2019).…”