Hormone-mediated maternal effects in birds:mechanismsmatter but what do we know of them?

Abstract

Over the past decade, birds have proven to be excellent models to study hormone-mediated maternal effects in an evolutionary framework. Almost all these studies focus on the function of maternal steroid hormones for offspring development, but lack of knowledge about the underlying mechanisms hampers further progress. We discuss several hypotheses concerning these mechanisms, point out their relevance for ecological and evolutionary interpretations, and review the relevant data. We first examine whether maternal hormones can accumulate in the egg independently of changes in hormone concentrations in the maternal circulation. This is important for Darwinian selection and female physiological trade-offs, and possible mechanisms for hormone accumulation in the egg, which may differ among hormones, are reviewed. Although independent regulation of plasma and yolk concentrations of hormones is conceivable, the data are as yet inconclusive for ovarian hormones. Next, we discuss embryonic utilization of maternal steroids, since enzyme and receptor systems in the embryo may have coevolved with maternal effect mechanisms in the mother. We consider doseresponse relationships and action pathways of androgens and argue that these considerations may help to explain the apparent lack of interference of maternal steroids with sexual differentiation. Finally, we discuss mechanisms underlying the pleiotropic actions of maternal steroids, since linked effects may influence the coevolution of parent and offspring traits, owing to their role in the mediation of physiological trade-offs. Possible mechanisms here are interactions with other hormonal systems in the embryo. We urge endocrinologists to embark on suggested mechanistic studies and behavioural ecologists to adjust their interpretations to accommodate the current knowledge of mechanisms.

Yolk androgens do not appear to mediate sexual conflict over parental investment in the collared flycatcher Ficedula albicollis

“…Second, increasing yolk androgen levels should either impose a cost or be constrained, since otherwise all females could afford to allocate high levels of androgens (e.g. Groothuis et al, 2005a;Groothuis and Schwabl, 2008). Indeed, elevated levels of androgens in the yolk can be costly for the chicks, as an immunosuppressive effect of androgens has been reported in some studies (e.g.…”

“…Moreover, such elevated levels may require elevated circulating androgen levels in the female, which may, for example, delay or inhibit egg laying (e.g. Clotfelter et al, 2004;Rutkowska et al, 2005; discussed in Groothuis and Schwabl, 2008). Finally, females should be able to respond differently to the chick trait influenced by yolk androgens than males.…”

“…However, whether the effects of the two hormones differ is uncertain, and their affinity to receptors is likely to differ (e.g. Groothuis and Schwabl, 2008). Therefore, we also examined the effects of each hormone separately and report the results when they clearly differ for the two hormones.…”

Examining a pathway for hormone mediated maternal effects – Yolk testosterone affects androgen receptor expression and endogenous testosterone production in young chicks (Gallus gallus domesticus)

“…Furthermore, hormone deposition varies systematically between species, but also between females of the same species or between and within clutches of the same mother (for reviews see [16,22,53]). These differences are assumed to be adaptive by shaping the offspring for its future environment [22,24]. Elevation of yolk androgen levels before incubation affect offspring morphology, begging behavior, competitiveness, growth, immune function, metabolic rate, hatching time and survival (for reviews see [16,17,22,39,53]).…”

Early growth conditions, phenotypic development and environmental change

“…In avian studies, most effort so far, at least outside of the poultry field, has gone into examining the consequences for chicks of maternally derived androgens in eggs. These are influenced by maternal state, and have substantial effects on chick growth and development (see Groothuis & Schwabl 2008;McGlothlin & Ketterson 2008). However, the extent to which maternal androgens provide environmental signals for the developing offspring, 'preparing' it for the environment it is most likely to encounter after fledging, has received little attention.…”