Wendt Müller

Sex differences in yolk hormones depend on maternal social status in Leghorn chickens ( Gallus gallus domesticus )

Maternal hormones are known to be present in avian eggs and can have beneficial effects on chick development. Recently, differences in avian yolk steroid concentrations between the sexes have been demonstrated, and in this context steroids have been proposed to be part of the avian sex–determining mechanism. In our study, we show that it is very unlikely that androgen concentrations alone are the decisive part of the sex–determining mechanism. We found that sex–specific differences in the yolk hormones strongly depend on the social rank of the mother. First, dominant females, but not subdominant females, allocated significantly more testosterone to male eggs than to female eggs. Second, subordinate females increased the testosterone concentrations of female eggs. This pattern of yolk hormone deposition can be functionally explained. In polygynous species such as the chicken, reproductive success is more variable in males than in females. Parental investment in sons or daughters is therefore expected to occur in direct relation to parental rearing capacities. We found that the social status of a hen was indeed negatively correlated with her maternal capacities (for example, body mass, egg mass). Differential androgen deposition might thus provide a mechanism for adaptive maternal investment depending on both the sex of the egg and the social status of the mother.

Avian mothers create different phenotypes by hormone deposition in their eggs

An increasing number of studies in a variety of taxa demonstrate the role of maternal sex steroids on offspring development. In avian species, mothers deposit substantial amounts of androgens in their eggs, and experimental evidence indicates that these maternal androgens influence the chicks early development. Despite the well-known organizing role of sex steroids on brain and behaviour, studies on avian maternal egg hormones almost exclusively focus on the chick phase. Here, we show experimentally that in Black-headed gulls maternal androgens in the egg enhance the development of the nuptial plumage and the frequency of aggressive and sexual displays almost 1 year after hatching. We conclude that maternal sex steroids may be a key factor for the determination of subtle but important individual differences within the same sex and species, which may have important consequences for Darwinian fitness and evolutionary processes.

Manipulative Signals in Family Conflict? On the Function of Maternal Yolk Hormones in Birds

Maternal hormones in the yolk of birds’ eggs have been a focus of attention in behavioral and evolutionary ecology stimulated by the pioneering work of Hubert Schwabl. Since then, knowledge of both the factors that influence maternal deposition patterns and their consequences for offspring development has accumulated rapidly. To date, the field has been dominated by the idea that mothers use yolk hormones to adaptively adjust offspring development, a view that assigns control over hormone deposition and its effects on the offspring to the mother. This neglects the possibility that the evolutionary interests of the mother and offspring differ. When there is such parent‐offspring conflict, the offspring are selected to respond to the hormones in a way that is adaptive for themselves rather than for the mother. Moreover, sexual conflict between the parents over parental investment may shape the evolution of yolk hormone deposition: females may manipulate the male’s contribution to parental care through the effect of yolk hormones on offspring begging, competitiveness, and developmental rate. We therefore suggest that for a full understanding of the evolution of hormone‐mediated maternal effects, it is essential to study both fitness consequences and physiological mechanisms and constraints from the perspective of all family members.

Yolk testosterone, postnatal growth and song in male canaries

Avian eggs contain substantial amounts of maternal yolk androgens, which have been shown to modulate offspring phenotype. The first studies on the functional consequences of maternal yolk androgens have focused on early life stages and their role in sibling competition. However, recent longitudinal studies reported long-lasting effects of maternal yolk androgens on offspring phenotype, mostly concerning traits that are sensitive to androgens. This suggests that maternal yolk androgens could play an important role in sexual selection, since the expression of many male sexual characters is testosterone-dependent. Using male canaries as a model, we examined the consequences of an experimental elevation of yolk testosterone concentrations on early development as well as long-lasting effects particularly on song, which is one of the most important sexual characters in male songbirds. Elevated yolk testosterone concentrations inhibited male growth, possibly in interaction with an existent ectoparasite exposure. Males hatched from testosterone-treated eggs (T-males) did not have enhanced competitive skills, in contrast to previous studies. The elevation of yolk testosterone concentrations delayed song development but did not affect adult song phenotype. This is intriguing, as yolk testosterone possibly induced developmental stress, which is known to reduce song quality. We hypothesize that yolk testosterone has either no direct effect on adult song phenotype, or that positive effects are merged by the negative effects of developmental stress. Finally, females mated with T-males invested more in their clutch indicating that females either assess T-males as more attractive (differential allocation hypothesis) or compensated for lower offspring viability (compensation hypothesis).

Elevated yolk androgen levels and the expression of multiple sexually selected male characters

Maternal hormones in bird eggs modulate not only offspring development, but recently it has also been shown that these effects can persist into adult life. A number of long-lasting effects concern traits of which the expression or development is modulated by androgens. This suggests that the nature of yolk hormone-mediated maternal effects may be organizational. Maternal androgens may therefore play an important role in sexual selection, since the expression of sexually selected male characters is often androgen-dependent. We experimentally manipulated the yolk androgen concentrations of European Starling (Sturnus vulgaris) eggs. Subsequently we followed 49 unrelated males from hatching until year of first reproduction. We investigated the expression of multiple sexually selected male characters (song, beak color and throat feather characteristics), taking into account whether a trait is androgen-dependent. Elevated levels of yolk androgens affected the length of the embryonic period, but did not modify the expression of either androgen-dependent or androgen-independent sexually selected male characters including song phenotype at adulthood. Thus the most important function of yolk androgens in starlings and possibly other bird species may relate to the early developmental period. The outcome of our study together with the results of our meta-analysis indicates that the effects of yolk androgens on sexually selected male characters may be comparatively small. Our results suggest that this may relate to the numerous other environmental and/or genetic factors influencing the expression of sexually selected male characters.

Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks

Avian eggs contain substantial amounts of maternal androgens. The concentrations of these yolk androgens are affected by the maternal environment, such as the level of social competition, parasite exposure or food conditions. Since yolk androgens have been shown to affect a wide array of offspring traits, they may adjust the chicks to the expected post-hatching environment, but experimental evidence is still scarce. We investigate in colonial breeding black-headed gulls whether high concentrations of yolk androgens, such as those found in environments with high numbers of social interactions, facilitate aggressiveness and territorial behaviour of the chicks. Black-headed gulls are highly suitable for this, as the semi-precocial chicks defend the natal territory and food against intruders. We manipulated yolk androgen concentrations and investigated their role in both within-nest and between-nest aggression. We found that chicks hatching from androgen-treated eggs defended the natal territory more often than their nest mates from control eggs, without increasing sibling aggression. This suggests that variation in yolk androgen concentrations in relation to the social environment of the mother may indeed allow adjustment of the offsprings behaviour to the expected frequency of territorial interactions with conspecifics post-hatching.

Long-lasting consequences of elevated yolk testosterone levels on female reproduction

Maternal yolk androgens in bird eggs represent an important pathway along which offspring phenotype is shaped. Most of the hormone-mediated maternal effects are highly important in the context of sibling competition. However, there is also increasing evidence for long-lasting effects far beyond the nestling period, and these effects may have important consequences on the reproductive success of the offspring. Here, we investigated the effects of experimentally elevated yolk testosterone concentrations on growth and reproduction in female canaries. Elevated yolk testosterone concentrations enhanced the post-natal growth rate, but not the asymptotic mass, and reduced the survival probability. The latter may be a consequence of the higher growth rate, which may have rendered females hatching from testosterone-treated eggs (T-females) more vulnerable to harsh environmental conditions. Adult T-females made a larger investment in their clutch by laying more but not heavier eggs than females hatching from control-treated eggs. Our results suggest that the observed long-lasting effect on clutch size relates to changes in the growth trajectory rather than being a direct consequence of testosterone, since studies manipulating early growth conditions obtained similar results. Clearly, further studies are now required in order to investigate the intriguing relationship between yolk testosterone, elevated growth rates, and clutch size.

Food conditions affect yolk testosterone deposition but not incubation attendance

In many bird species with hatching asynchrony, yolk androgens increase across the laying sequence. This has been hypothesized to represent a compensatory mechanism for disadvantages of later-hatching chicks - via positive effects of yolk androgens on early competitiveness and growth. However, the costs and benefits of this compensatory strategy probably depend on environmental factors determining the survival chances of the chicks such as the food conditions, which should, therefore, influence maternal yolk androgen deposition. We studied the consequences of manipulated food conditions on the expected level of hatching asynchrony in canaries (Serinus canaria) assigning females to either a low (=LQ) or high quality (=HQ) diet. We measured the incubation behaviour (as incubation attendance) and the yolk androgen deposition in order to investigate whether and how females modulate hatching asynchrony in relation to the food conditions. Females on a HQ diet laid larger and heavier clutches, showed a stronger increase in yolk testosterone content towards the last-laid eggs, but did not alter their incubation attendance. Thus, females on a HQ diet seem to favour the survival of later hatching chicks, as indicated by their yolk testosterone deposition pattern. However, females on a HQ diet laid larger clutches and might need to compensate more in order to achieve a similar degree of hatching asynchrony than females on a LQ diet, given the lack of plasticity in incubation attendance. This suggests that canary females respond to food manipulations mainly via changes in clutch size rather than by altering the degree of hatching asynchrony.

Coadaptation of offspring begging and parental provisioning--an evolutionary ecological perspective on avian family life.

Offspring begging and parental provisioning are the two central social behaviours expressed during the period of parental care. Both behaviours influence each other and it is, therefore, hypothesized that they should ultimately become (genetically) correlated, stabilized by fitness costs to parents and/or offspring. By reciprocally exchanging entire clutches in canaries (Serinus canaria), we tested (1) whether there is covariation between these behaviours and (2) whether a mismatch - as introduced by cross-fostering - entails costs. Begging was scored in a standardized begging test and parental provisioning was measured via (a) the actual feeding rate and (b) using the growth rate of the foster nestlings as a proxy. Costs were established in terms of future reproductive investment in subsequent clutches and offspring growth. We found a positive and significant phenotypic covariation between offspring begging and parental feeding when using the growth rate as a proxy and, to a lesser extent, in case of the parental feeding rate. Female parents suffered no future reproductive costs when feeding foster nestlings that were more demanding than their own nestlings. Neither growth measured amongst all offspring nor the reproductive investment measured amongst the female offspring as adults was influenced by their begging behaviour. However, the reproductive investment of female offspring tended to depend on the parental qualities of their foster parents. Thus, offspring may only be able to extract resources within the limit of generosity of their foster parents. This suggests parental control of feeding, which is also supported by the positive covariation between offspring begging and parental feeding.

GnRH--a missing link between testosterone concentrations in yolk and plasma and its intergenerational effects.

Despite the strong interest in hormone-mediated maternal effects two key questions concerning their mechanisms are as yet unanswered: First, whether the deposition of hormones in the egg yolk is coupled with the levels of these hormones in the maternal circulation, and second, whether epigenetic changes as induced by embryonic exposure to maternal yolk hormones impinge on yolk hormone deposition at adulthood. We investigated the responsiveness to gonadotropin-releasing hormone (GnRH) in female canaries whose embryonic exposure to yolk testosterone had been manipulated. This enabled us to study to what extent GnRH interlinks testosterone concentrations in female circulation and egg yolk as well as the intergenerational potential of hormone-mediated maternal effects. As expected, canary females responded to GnRH with a rise in plasma testosterone. The GnRH-responsiveness was positively correlated with the yolk testosterone content. Factors stimulating the release of GnRH will, therefore, lead to an increase of testosterone in both plasma and egg, posing a potential constraint on the yolk hormone deposition due to testosterone related trade-offs within the laying female. Exposure to elevated yolk testosterone levels as embryo reduced the GnRH-responsiveness in adulthood, potentially limiting environmental influences on yolk testosterone deposition, but the concentrations of yolk testosterone itself were not affected.