Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model

Abstract

Maternal effects can adaptively modulate offspring developmental trajectories in variable but predictable environments. Hormone synthesis is sensitive to environmental factors, and maternal hormones are thus a powerful mechanism to transfer environmental cues to the next generation. Birds have become a key model for the study of hormone-mediated maternal effects because the embryo develops outside the mother's body, facilitating the measurement and manipulation of prenatal hormone exposure. At the same time, birds are excellent models for the integration of both proximate and ultimate approaches, which is key to a better understanding of the evolution of hormone-mediated maternal effects. Over the past two decades, a surge of studies on hormone-mediated maternal effects has revealed an increasing number of discrepancies. In this review, we discuss the role of the environment, genetic factors and social interactions in causing these discrepancies and provide a framework to resolve them. We also explore the largely neglected role of the embryo in modulating the maternal signal, as well as costs and benefits of hormone transfer and expression for the different family members. We conclude by highlighting fruitful avenues for future research that have opened up thanks to new theoretical insights and technical advances in the field. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.

Testing for context-dependent effects of maternal thyroid hormones on offspring survival and physiology: an experimental approach manipulating temperature in a wild bird species

“…Maternal effects may translate environmental cues from the mother to the offspring for example via maternally transferred hormones (hereafter 'maternal hormones'), potentially increasing offspring survival in the predicted conditions (adaptive maternal effects, 1,[2][3][4]. Maternal hormone-mediated effects have been recently highlighted as a potential mechanism and source of phenotypic plasticity to respond to changing climate (5)(6)(7), yet empirical evidence is scarce.…”

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

“…A challenge faced in this study is that the actual concentration of corticosterone transferred from the mother to egg remains largely unknown (Rettenbacher et al, 2009, 2013a; Almasi et al, 2012) and may differ across strains (Navarra and Pinson, 2010). Although analytical techniques such as Celite and HPLC are more precise than the often used enzyme- and radio-immunoassay, they may still not be sufficiently accurate to quantify the concentration of corticosterone in the yolk (reviewed in Groothuis et al, (23)). Therefore, the hormone concentration used in our injections might have been lower than the physiological range of different strains of breeder hens, thus explaining the negative findings.…”

“…The mean concentration of corticosterone in eggs from unstressed birds has been previously reported as 1.17 in yolk and 1.55 ng/mL albumen (40). However, analytical validation of enzyme- and radio-immunoassay techniques showed the presence of cross-reactive substances that hamper quantification of corticosterone in the yolk and albumen of eggs (41); and recent work has shown that even more precise techniques such as Celite or high performance liquid chromatography may not be sufficient to accurately quantify the corticosterone concentration in yolk (reviewed in Groothuis et al, (23)). Therefore, since the exact concentration of corticosterone in eggs from stressed birds remains unknown, we followed the methodology proposed by Janczak et al (42) and described in Peixoto et al (17), that was based on plasma corticosterone concentration of stressed hens.…”

“…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.…”

Testing different forms of regulation of yolk thyroid hormone transfer in pied flycatchers

“…Maternal effects are the non-genetic influences of a mother on her progeny and are thought to 36 be adaptive (Moore et al, 2019;Mousseau and Fox, 1998;Yin et al, 2019). Maternal 37 hormones transferred to the next generation are a potential prenatal pathway for mothers to 38 shape their offspring phenotype (Groothuis et al, 2005;Groothuis et al, 2019;Ruuskanen 39 and Hsu, 2018, 20). Mothers transfer thyroid hormones (THs) that have so far received little 40 attention compared to glucocorticoids and androgens .…”