News and Comment

Testosterone and maternal effects – integrating mechanisms and function

The development of individual behavioural profiles can be powerfully influenced by stressful social experiences. Using a comparative approach, we focus on the role of social stressors for the modulation of behavioural profile during early phases of life and adolescence. For gregarious species, the stability of the social environment in which the pregnant and lactating female lives is of major importance for foetal brain development and the behavioural profile of the offspring in later life. Social instability during these critical periods of development generally brings about a behavioural and neuroendocrine masculinisation in daughters and a less pronounced expression of male-typical traits in sons. Moreover, when mothers live in a socially threatening world during this time, anxiety-like behaviour of their offspring often is elevated in adulthood. These effects of the social environment are likely to be mediated by maternal hormones and/or maternal behaviour. In addition, they can be modulated significantly by offspring genotype. We favour the hypothesis that the behavioural effects of social stress during this phase of life are not necessarily “pathological” (nonadaptive) consequences or constraints of adverse social conditions. Rather, mothers could be adjusting the offspring to their environment in an adaptive way. Adolescence is another period in which behavioural development is particularly susceptible to social influences. There is some evidence that stressful social events experienced at this time alter and canalize behaviour in an adaptive fashion, so that earlier influences on behavioural profile development can be complemented and readjusted, if necessary, to meet current environmental conditions. In terms of underlying neuroendocrine mechanism, a central role for the interaction of testosterone and stress hormones is suggested. In summary, the modulation of behavioural profiles by social stress from the prenatal phase through adolescence appears to represent an effective mechanism for repeated and rapid adaptation.

This chapter reviews maternal hormones in avian eggs, their effects, their regulating mechanisms, and their potential Darwinian function, i.e., the way in which they maximize survival and reproductive success. An avian egg contains all the substances needed to produce a fully functioning organism. In addition to basic resources (proteins, lipids, water, and minerals), eggs contain a range of other substances, such as vitamins, antibodies, and enzymes. These appear to fulfill important functions, acting as regulators of embryonic development and protecting the embryo against pathogens, or may represent metabolic waste products. The eggs also contain substantial levels of maternal hormones. Their levels vary in relation to a range of factors such as laying order, food availability, breeding density, and male quality. Yolk hormones subsequently influence offspring growth, behavior, physiology, immune system, and ultimately survival and reproduction. Separate control over hormone levels in circulation and yolk allows independent effects on offspring and mothers, while regulation of the response to maternal hormones allows offspring to fine-tune the effects on different traits.

It is widely believed that female birds strategically allocate androgens to yolk in the manner that best equips offspring for feeding conditions during their development. Because most avian studies have focused on multi-egg clutch species, and interpreted results within the framework of sibling competition, we still know little about how yolk androgens might be allocated in direct response to environmental conditions. Most oceanic birds are long-lived and lay single-egg clutches, and their breeding success is tightly linked to highly variable marine production. That combination: a variable breeding environment, long lives, and single-egg clutches, makes oceanic birds good subjects to test hypotheses about yolk androgen allocation strategies. We measured concentrations of two yolk androgens, androstenedione (A4) and testosterone (T), in the single-egg clutches laid by early-laying Cassin’s (Ptychoramphus aleuticus) and rhinoceros (Cerorhinca monocerata) auklets at Triangle Island, British Columbia, Canada, in 2002–2004. Environmental conditions including sea-surface temperatures and the timing and intensity of marine primary production varied over the 3 years, and in response, both the timing and success of seabird breeding varied. As in other avian species, concentrations of A4 and T varied markedly among individual eggs in both species (by factors of 3–8), yet contrary to expectation, little of the variation could be attributed to year effects. The high interindividual variation and the lack of interannual variation suggest a non-adaptive explanation for yolk androgen deposition relative to environmental conditions in these species.

This chapter discusses the physiology, ecology, and behavior of hormones in avian eggs. The main source of hormones found in avian eggs is the maturing follicles of the female ovary that contain specialized cells creating different hormones during their development. The granulosa cells of the largest preovulatory follicles (F1) are the main source of circulating progesterone. Theca cells produce both estrogen and androgens, and the production decreases with increasing follicular maturation. Postovulatory follicles continue to produce steroids before final atresia, and their low androgen production during incubation is brought about by a decrease in luteinizing hormone stimulation rather than by a reduction of the steroidogenic capacity of the theca interna cells at that stage. Although sexual differentiation takes place in the early embryo by the means of processes based on estradiol, the development of sexually selected characters in birds is tightly linked to hormonal processes in adulthood, of both androgenic and estrogenic nature. While within‐brood distributions of yolk androgens can be highly species‐specific, many differential patterns can be found within the same species. Given the effects of androgens in chick competitiveness, females could use within‐clutch distributions of androgens to balance or reinforce the effects of hatching asynchrony.

In mammals, prenatal social stress results in a behavioral and neuroendocrine masculinization in female offspring and a less pronounced expression of male-typical traits in male offspring. Maternal androgens are involved in mediating these effects by shaping fetal brain development. This could signify an adaptive behavior by the mother adopted to adjust her offspring to the current environmental conditions.

In this review, we summarise experimental animal studies on the effects of the social environment during pregnancy on the offsprings' behaviour, brain, and neuroendocrine function. We show that in non-human mammals the stability of the social environment in which the pregnant females live is critical for the offsprings' social and sexual behaviour later in life as well as for reproductive functioning, endocrine state and androgen and estrogen receptor distribution in specific parts of the brain. Based on these findings, we discuss different neuroendocrine mechanisms mediating the influence of the social environment during pregnancy on the offsprings' behaviour. We conclude that maternal steroids play a decisive role in shaping foetal brain development. However, a pituitary adrenocortical pathway need not always be involved. At least in some cases an involvement of the sympathetic adrenomedullary system seems to be possible. Concerning function, we favour the hypothesis that the behavioural effects of prenatal social stress are not necessarily the ‘pathological’ consequences of adverse social conditions (non-adaptive explanation). Contrarily, mothers could be adjusting their offspring to the environment in which they live during pregnancy in an efficient way (adaptive explanation).