Hormone mediated maternal effects in birds

Apart from genetic inheritance, parents, and especially the mother, can influence offspring development by the transfer of non-genetic material. As the avian embryo develops in a sealed environment, eggs provide an excellent model to study these non-genetic effects. Recent studies on hormone-mediated maternal effects in birds have highlighted the influence of variable yolk steroid hormone concentrations on offspring phenotype (morphology, physiology and behaviour). The concentrations of steroid hormones in egg yolk are modulated by various environmental conditions. Despite numerous studies on these so-called epigenetic effects, the underlying physiological mechanism allowing the female to manipulate yolk hormone concentrations has hardly been elucidated so far. In birds, interactions between stress and reproductive hormones are well-investigated, however, a possible influence of glucocorticoids (GCs) on the follicular synthesis of gonadal steroids and their deposition into the egg has not been explored yet. We hypothesise that elevated plasma GC concentrations of the mother trigger changes in phenotypic properties of her offspring and that this effect is mediated via maternally derived steroid hormones of gonadal origin, which are deposited into the yolk. In the presented study, the consequences of experimentally elevated maternal plasma corticosterone concentrations on yolk steroid hormone concentration and offspring development (physiology and behaviour) will be elucidated. Insight into the underlying physiological mechanism of hormone deposition would greatly benefit the functional and evolutionary approach to the quickly expanding research field. The combination of stress physiology and hormone mediated maternal effects and the analyses of both the causal mechanism and functional consequences will have a broad impact as the field of hormone mediated maternal effects in birds urgently requires input about its underlying physiological mechanisms. This would greatly support the understanding of proximate and ultimate causes of hormone mediated maternal effects in birds.

Since maternal stress affects offspring in birds, it has been assumed that corticosterone is directly transferred from the female`s plasma to her eggs and that yolk concentrations simply reflect females` plasma concentrations. The finding of high corticosterone concentrations in yolks of several bird species seemed to support this assumption. Until today however, there has been no proof that corticosterone was measured in those samples. According to our findings, the reported measurements do not relate to authentic yolk corticosterone, but are in fact caused by cross- reactions: Quantification of yolk corticosterone is confounded by the high amounts of gestagens present in the yolk (progesterone, pregnenolone and others). Gestagens can bind to any corticosterone antibody and give a signal in a corticosterone immunoassay. In fact, avian eggs contain only minor amounts of glucocorticoids. The biological relevance of these low concentrations remains elusive, especially because bird embryos are able to degrade corticosterone into metabolites during incubation. A direct influence of maternal corticosterone on the bird embryo therefore seems unlikely but maternal stress in birds has still been shown to generate different offspring phenotypes. We therefore investigated a more indirect communication of maternal stress to the bird embryo. As glucocorticoids can affect reproductive hormones, we tested the influence of corticosterone on the production of gonadal steroids such as androgens and gestagens and their deposition into the egg, as androgens in the egg have been shown to profoundly affect birds` behaviour and physiology. Our results indicate that corticosterone suppresses steroid production of the avian follicles, resulting in eggs that contained fewer androgens and gestagens. Chicks that hatched from these eggs were smaller, less competitive and their immuneresponse was downregulated. We conclude that an increase of a bird mothers` plasma corticosterone concentrations could trigger changes in phenotypic properties of her offspring by influencing the amount of gonadal steroid hormones that are deposited into the yolk. This might explain the environmentally induced variation of yolk androgen concentrations, which are frequently reported in bird species. We also conclude that maternal stress is mediated indirectly to the offspring via decreasing the amount of maternal androgens and gestagens in the egg yolk. Similar to mammals, avian embryos seem to be protected against direct effects of maternal corticosterone.