Yolk Androgens Research Articles

Early conversion of maternal androgens affects the embryo already in the first week of development.

Maternal androgen exposure has potent effects on offspring development. As substantial levels of maternal androgens are deposited in avian egg yolks, avian eggs are frequently used to study maternal effects, with a strong focus on post-natal development. However, the underlying pathways are largely unknown. Since the hormones are taken up during the embryonic phase, and these are rapidly metabolized by avian embryos into metabolites such as etiocholanolone, we studied the effects of yolk androgens (testosterone and androstenedione) and their metabolite etiocholanolone during the first few days of embryonic development. As embryonic heart rate is often used as an indicator of embryonic development, we measured the heart rate from day 3 to day 6 of incubation by using a shell-less culture technique in rock pigeon eggs (Columba livia). Increased androgen exposure increased heart rate, and increased etiocholanolone mimicked this effect, albeit in a small sample size. This indicates that exposure to maternal androgens increases embryonic overall metabolism which may account for the developmental outcomes found in previous studies such as increased growth. Moreover, etiocholanolone is likely to be an important metabolite in a non-genomic pathway underlying the androgen-mediated maternal effect.

Embryonic heart rate is affected by yolk androgens and egg laying sequence, and correlates with embryonic tissue growth: A study in rock pigeons

Maternal androgen exposure can have crucial effects on offspring development. Bird eggs are frequently used for studying these effects and virtually all research in this field has focused on post-hatching offspring traits. Yet, much of the yolk, in which the maternal hormones are deposited, is consumed during the embryonic phase. Here, we studied the effects of yolk androgens during this prenatal period. As there is evidence that androgens stimulate post-hatching traits such as increased growth, we measured heart rate throughout incubation as a proxy for prenatal metabolism. Rock pigeons (Columba livia) typically lay 2-egg clutches with yolk androgen levels in second-laid eggs being consistently higher than in first-laid eggs. We investigated whether embryonic heart rate was higher in second- than first-laid eggs. Additionally, we increased yolk androgen levels (testosterone and androstenedione) with the mean difference between those in first- and second-laid eggs, to investigate whether the effects of androgens are egg sequence dependent. As expected, embryonic heart rate predicted body embryo organ- and body mass, and body dimensions, with body mass being significantly higher in second- than first-laid eggs. Androgen treated first-laid eggs increased heart rate to that of second-laid control eggs only temporally, yet it had an overall positive effect on embryo body dimensions but not on tissue mass. Our findings indicate that embryos from different egg laying sequence differed in heart rate and prenatal development outcomes but this can only partially be explained by their difference in maternal androgen levels.

Nest predation risk and deposition of yolk steroids in a cavity-nesting songbird: an experimental test.

Maternal hormones can shape offspring development and increase survival when predation risk is elevated. In songbirds, yolk androgens influence offspring growth and begging behaviors, which can help mitigate offspring predation risk in the nest. Other steroids may also be important for responding to nest predation risk, but non-androgen steroids have been poorly studied. We used a nest predator playback experiment and liquid chromatography with tandem mass spectrometry (LC-MS-MS) to assess whether nest predation risk influences deposition of 10 yolk steroids. We found no clear evidence that yolk androgen deposition changed when perception of nest predation risk was experimentally increased. However, elevated nest predation risk led to decreased yolk progesterone deposition. Overall, our results suggest yolk progesterone may be more important than yolk androgens in responses to offspring predation risk and highlight new avenues for research.

Prenatal manipulation of yolk androgen levels affects egg size but not egg colour in a songbird

Maternal allocation of androgens to the egg yolk allows mothers to adaptively manipulate offspring phenotype. Increases of egg androgen levels have often been shown to induce sex-specific effects. Some previous studies suggest that females specifically may suffer a fitness reduction after early exposure to high androgen levels. In this study, we explored whether female birds that developed exposed to high yolk androgen concentrations would reduce their maternal investment later in life. We explored two different aspects of female reproduction in spotless starlings (Sturnus unicolor): egg coloration (a post mating sexual signal in this species) and egg size. We manipulated androgen yolk levels in a large sample of clutches of this species. We monitored the reproduction of the females that hatched from these eggs, measuring the size and colour of the eggs they laid throughout their life (from 1 to 7 years of age). We found no overall difference in egg colour in relation to treatment, clutch number or age. However, females exposed to high egg androgen levels showed a steeper decrease in egg size along the laying order than controls. This pattern likely results in a more unbalanced distribution of resources within the clutch, possibly favouring brood size reductions in experimental females. In addition, control and experimental females differed in how egg volume changed with age. These results show that some egg characteristics may be affected by the female’s exposure to yolk androgens during her own embryonic development. Our research calls for further long-term research on the influence of prenatal androgens on the fitness mechanisms regulating reproductive investment and its potential signalling role in a perspective of sexual selection. In birds, mothers prepare the offspring to the environment they will encounter at hatching by depositing a mixture of compounds into the eggs. Androgens specifically exert a variety of effects during embryo development and chick growth, but some of these may be negative in adult life. In particular, early androgen may be detrimental for females in the long term, decreasing maternal investment and fitness. Using the spotless starling as study species, we tested whether an experimental increase in yolk androgens negatively affects breeding investment, measured by egg colour (a sexual signal) and egg size. We found no effects of the treatment on egg colour. However, females exposed to high androgen levels during their development reduced egg size along the laying order more strongly than controls. This may affect nestling survival, and indicates that prenatal yolk androgens may influence some egg characteristics with known relevance for offspring viability.

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds.

Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro‐evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α‐dihydrotestosterone [5α‐DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex‐dependent for T); (c) greater among‐female variation of yolk T and 5α‐DHT concentrations in the forest than city population, but similar within‐clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population‐specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone‐mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population‐specific relationships rather than trade‐off against each other.

Age-related patterns of yolk androgen deposition are consistent with adaptive brood reduction in spotless starlings

Female birds can influence offspring development by adjusting egg size or by a differential allocation of egg resources. Such maternal effects can be expected to be shaped by natural selection, given the costs connected to the allocation of maternal resources. Among egg components, yolk androgens play an important role in affecting offspring life-history traits. Despite their relevance for nestling development, factors accounting for the observed within- and between-clutch variation are still poorly known. By using a cross-sectional sampling approach, we tested the effect of female age, laying order and laying date on the deposition of yolk androstenedione (A4) and testosterone (T), since young and older females could maximize their fitness differently according to breeding conditions. We found a remarkable lack of differences in overall yolk androgen levels across different ages. However, comparing first-year with older females, our results showed that age did not influence yolk T levels at the beginning of the breeding season, whereas at the end, first-year females transferred lower hormone levels than older females. Within clutches, both androgens increased across the laying sequence, suggesting that late nestlings benefit from an increased allocation that could compensate hatching asynchrony. However, when considering A4, we found that, whereas older females always increased A4 levels across the laying sequence, first-year females did not increase it at the end of the breeding season, thus increasing the likelihood of brood reduction when environmental conditions became hardest. These findings suggest that yolk A4 variation may be particularly important at the within-clutch scale, by providing females with a tool to modify nestling hierarchies. The study of maternal effects shows that avian mothers can adjust offspring development to environmental conditions by altering egg composition. The effects of maternal age on such egg allocation process depend on the balance of benefits and costs that affects each age class. We examine if young and older mothers differ in terms of yolk androgen deposition and egg quality, since age may influence offspring fitness, and could represent a costly maternal investment. We found an absence of overall age-dependent patterns in yolk androgen deposition, except when we considered laying order and laying date. In late clutches, when breeding conditions are harsher, 1-year-old females carried out a lower deposition of both resources (yolk mass) and modifiers (androgens) than older mothers did. We suggest that such a pattern would reinforce the effects of hatching asynchrony, favouring brood reduction at the end of the breeding season by first-year females.

Does paternal immunocompetence affect offspring vulnerability to maternal androgens? A study in domestic chickens.

ABSTRACTExposure of yolk androgens can positively stimulate chick growth and competitive ability, but may negatively affect immunity. It has been hypothesized that only chicks from immunologically superior fathers can bear the cost of prenatal exposure to high androgen levels. To test this hypothesis, we paired roosters from two selection lines, one up- and one down-selected for natural antibodies (NAbs), with hens from a control line. We measured yolk testosterone and androstenedione levels, and we injected the treatment group of eggs of each female with testosterone suspended in sesame oil and the control group with sesame oil only. We then measured hatching success and growth, and characterized the humoral and cellular immune responses using three different challenges: a phyto-hemagglutinin, a lipopolysaccharide and a sheep red blood cell challenge. We found that the hatching success, body mass, initial levels of natural antibodies and the chicks’ immunological responses to the three different challenges and development were affected neither by paternal immunocompetence nor by treatment. These results do not support the hypothesis that chicks from low-NAb line fathers are more sensitive to testosterone exposure during embryonic development than chicks from high-NAb line fathers.

The relationship between male social status, ejaculate and circulating testosterone concentration and female yolk androgen transfer in red junglefowl (Gallus gallus)

Several studies show that avian females prefer males based on their secondary sexual ornaments and dominance status. We tested in red junglefowl (Gallus gallus) how comb size affected the result of fighting and how the dominance status related to testosterone concentrations in their circulation and ejaculates. We subsequently tested how social status was related to female reproductive investment, including yolk hormone transfer. We found that after a fight 1) winners increased plasma T and decreased ejaculates T whereas losers' T remained unchanged, and 2) plasma T of winners was higher but ejaculates T was lower than those of losers. We argued those are consistent with the different reproductive strategies of dominant and subordinate males. Furthermore, in line with offspring sex-dependent growth patterns females transferred significantly more androstenedione to female than male embryos when mated with winners, while doing the opposite when mated with losers. We concluded therefore that female reproductive investment was affected by both partner quality and embryo sex. The results indicate that male quality influences sex-specific maternal investment, which could be mediated by ejaculate testosterone concentration.

Steroid receptors and their regulation in avian extraembryonic membranes provide a novel substrate for hormone mediated maternal effects

Exposure of the vertebrate embryo to maternal hormones can have long-lasting effects on its phenotype, which has been studied extensively by experimentally manipulating maternal steroids, mostly androgens, in bird eggs. Yet, there is a severe lack of understanding of how and when these effects are actually mediated, hampering both underlying proximate and ultimate explanations. Here we report a novel finding that the embryo expresses androgen receptor (AR) and estrogen receptor (ERα) mRNA in its extraembryonic membranes (EMs) as early as before its own hormone production starts, suggesting a novel substrate for action of maternal hormones on the offspring. We also report the first experimental evidence for steroid receptor regulation in the avian embryo in response to yolk steroid levels: the level of AR is dependent on yolk androgen levels only in the EMs but not in body tissues, suggesting embryonic adaptation to maternal hormones. The results also solve the problem of uptake of lipophilic steroids from the yolk, why they affect multiple traits, and how they could mediate maternal effects without affecting embryonic sexual differentiation.

Experimental increase in temperature affects eggshell thickness, and not egg mass, eggshell spottiness or egg composition in the great tit (Parus major)

Phenotypic effects of global warming have been documented in many different taxa. However, the importance of transgenerational phenotypic plasticity in these adaptations are seldom studied. In birds, temperature could affect egg characteristics. Higher temperatures during egg-laying may reduce maintenance costs for females and allow a higher investment in reproduction. Yet, females may also use temperatures as a cue for the risk of mismatch latter in the season. Thus, higher temperatures may be correlated to an acceleration of embryonic development (e.g. via hormonal manipulation). We performed an experiment in which night-time temperature was increased in the nestbox by approximately 1 °C throughout the entire laying period in great tits (Parus major). We collected one pre-treatment egg (beginning of the laying sequence) and one post-treatment egg (end of the laying sequence). Egg content (yolk androgens and lysozymes in the albumen), eggshell coloration, eggshell mass, egg mass, and shape were not affected by the treatment. However, last-laid eggs in clutches from control nestboxes had a thicker eggshell than last-laid eggs from heated nestboxes, suggesting a putative slight decrease of maternal investment with the experimental increase of temperature. We also observed effects of the laying sequence on egg characteristics. Eggs that were laid late in the laying sequence were heavier, larger, had larger spots and higher yolk androgens than eggs laid earlier. Lysozyme concentration decrease with the laying sequence in late clutches only. Thus, effects of temperature may also change with the laying sequence and it would be interesting in the future to tests the effects on first-laid eggs.

Avian yolk androgens are metabolized rather than taken up by the embryo during the first days of incubation.

Several studies show effects of yolk androgens in avian eggs on the phenotype of the offspring. Yolk hormone concentrations decline strongly within the first few days of incubation. Although early embryonic uptake of yolk androgens is suggested by the presence of radioactivity in the embryo when eggs are injected with radiolabelled androgens, these studies do not verify the chemical identity of radioactive compound(s), although it is known that these androgens can be metabolized substantially. By using stable isotope-labelled testosterone and androstenedione in combination with mass spectrometry, enabling verification of the exact molecular identity of labelled compounds in the embryo, we found that after 5 days of incubation the androgens were not taken up by the embryo. However, their concentrations in the entire yolk albumen homogenates declined strongly, even when corrected for dilution by albumen and water. Our results indicate metabolism of maternal androgens, very likely to 5β-androstane-3α,17β-diol, etiocholanolone and their conjugated forms. The results imply that the effects of increased exposure of the embryo to maternal androgens take place either before this early conversion or are mediated by these metabolites with an as yet unknown function, opening new avenues for understanding hormone-mediated maternal effects in vertebrates.

Maternal egg hormones in the mating context: The effect of pair personality

AbstractAnimal personality traits emerge developmentally from the interaction of genetic and early environmental factors. Maternal hormones, such as androgens (testosterone, T and androstenedione, A4), transferred to embryos and egg yolks may simultaneously organize multiple behavioural and physiological traits. Although previous studies demonstrated an association between the mother's personality and yolk androgen levels, the independent effects of the male partner's personality and pair combination remains unknown.We test this association using an ecological model species for personality research, the great tit (Parus major) using multiple approaches: (1) a wild population, (2) a randomly mated captive population and (3) an experimental study with (dis)assortatively mated pairs from lines selected for fast exploration/boldness or slow exploration/shyness.Egg androgen concentrations were associated with variation in female personality traits, and the experimental data suggested that this is independent of male personality: Experimental females from the slow‐shy line tended to have higher egg T concentrations than females from the fast‐bold line, with no effect of male personality. Shy females from the wild population had higher egg A4 concentration than bold females. However, in the correlative data yolk hormones were linked with male personality, as well as the interaction between female and male traits: Male handling responsiveness correlated negatively with egg A4 concentration in wild birds. In randomly mated birds, pairs that were mated assortatively for personality had lower egg T concentrations than disassortatively mated pairs.Given that egg androgens are known mediators of avian personality, our results suggest that maternal hormones might contribute to the heritability of personality, may be sensitive to the social context of mating, and act as key drivers of individual differences.Aplain language summaryis available for this article.

Sex-Specific Effects of High Yolk Androgen Levels on Constitutive and Cell-Mediated Immune Responses in Nestlings of an Altricial Passerine.

Avian embryos are exposed to yolk androgens that are incorporated into the egg by the ovulating female. These steroids can affect several aspects of embryo development, often resulting in increases in overall size or the speed of growth of different traits. However, several studies suggest that they also entail immune costs to the offspring. In this study, we explored whether variation in yolk androgen concentration affected several measures of the constitutive and cell-mediated immune axes in the spotless starling (Sturnus unicolor). Using a within-brood design, we injected different doses of androgens (testosterone and androstenedione) into the eggs. Our study showed that experimentally increased yolk androgens led to sex-specific immunosuppression in both the innate and adaptive axes of the immune system. Both cell-mediated immune response (CMI) and lysozyme activity decreased with increasing androgen levels injected into the egg in the case of male nestlings, whereas there were no effects on females. The effects that we found were always linear: no quadratic or threshold patterns were detected. We found no effects of the experimental treatment in hemolysis or agglutination capacity, but these measures were negatively correlated with CMI, suggesting negative correlation among different branches of the immune system. Blood (trypanosomes and hemosporidians) and intestinal (coccidia) parasites were not affected by the experimental increase of yolk androgen levels. Our results show that in our study species yolk androgens induce immunosuppression in some axes of the male nestling immune system. Further studies should analyze the proximate causes for these contrasting effects in different axes of the immune system and the reason for the differential impact on males and females.

Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors.

Maternal reproductive investment can critically influence offspring phenotype, and thus these maternal effects are expected to be under strong natural selection. Knowledge on the extent of heritable variation in the physiological mechanisms underlying maternal effects is however limited. In birds, resource allocation to eggs is a key mechanism for mothers to affect their offspring and different components of the egg may or may not be independently adjusted. We studied the heritability of egg components and their genetic and phenotypic covariation in great tits (Parus major), using captive-bred full siblings of wild origin. Egg mass, testosterone (T) and androstenedione (A4) hormone concentrations showed moderate heritability, in agreement with earlier findings. Interestingly, yolk triiodothyronine hormone (T3), but not its precursor, thyroxine hormone (T4), concentration was heritable. An immune factor, albumen lysozyme, showed moderate heritability, but yolk immunoglobulins (IgY) did not. The genetic correlation estimates were moderate but statistically nonsignificant; a trend for a positive genetic correlation was found between A4 and egg mass, T and lysozyme and IgY and lysozyme, respectively. Interestingly, phenotypic correlations were found only between A4 and T, and T4 and T3, respectively. Given that these egg components are associated with fitness-related traits in the offspring (and mother), and that we show that some components are heritable, it opens the possibility that natural selection may shape the rate and direction of phenotypic change via egg composition.

High Yolk Testosterone Transfer Is Associated with an Increased Female Metabolic Rate.

Yolk androgens of maternal origin are important mediators of prenatal maternal effects. Although in many species short-term benefits of exposure to high yolk androgen concentrations for the offspring have been observed, females differ substantially in the amount of androgens they transfer to their eggs. It suggests that costs for the offspring or the mother constrain the evolution of maternal hormone transfer. However, to date, the nature of these costs remains poorly understood. Unlike most previous work that focused on potential costs for the offspring, we here investigated whether high yolk testosterone transfer is associated with metabolic costs (i.e., a higher metabolic rate) for the mother. We show that Japanese quail (Coturnix japonica) females that deposit higher testosterone concentrations into their eggs have a higher resting metabolic rate. Because a higher metabolic rate is often associated with a shorter life span, this relationship may explain the negative association between yolk testosterone transfer and female longevity observed in the wild. Our results suggest that metabolic costs for the mother can balance the short-term benefits of yolk testosterone exposure for the offspring, thereby contributing to the maintenance of variation in maternal yolk hormone transfer in natural populations.

Temperature-induced variation in yolk androgen and thyroid hormone levels in avian eggs

Global warming has substantially changed the environment, but the mechanisms to cope with these changes in animals, including the role of maternal effects, are poorly understood. Maternal effects via hormones deposited in eggs, have important environment-dependent effects on offspring development and fitness: thus females are expected to adjust these hormones to the environment, such as the ambient temperature. Longer-term temperature variation could function as a cue, predicting chick rearing conditions to which yolk hormone levels are adjusted, while short-term temperature variation during egg formation may causally affect hormone transfer to eggs. We studied the effects of ambient temperature on yolk androgens (testosterone and androstenedione) and thyroid hormones (thyroxine and triiodothyronine) in great tits (Parus major) using data from unmanipulated clutches from a wild population and from aviary birds (ad libitum food) exposed to different experimental temperature treatments during five years. Both in the wild and in captivity, longer-term pre-laying ambient temperature was not associated with clutch mean yolk hormone levels, while the way androstenedione and thyroxine levels varied across the laying sequence did associate with pre-laying temperature in the wild. Yolk testosterone levels were positively correlated with short-term temperature (during yolk formation) changes within clutches in both wild and captivity. We also report, for the first time in a wild bird, that yolk thyroxine levels correlated with a key environmental factor: thyroxine levels were negatively correlated with ambient temperature during egg formation. Thus, yolk hormone levels, especially testosterone, seem to be causally affected by ambient temperature. These short-term effects might reflect physiological changes in females with changes in ambient temperature. The adaptive value of the variation with ambient temperatures pre-laying or during egg formation should be studied with hormone manipulations in different thermal environments.

Maternal transfer of androgens in eggs is affected by food supplementation but not by predation risk

Mothers may affect the future success of their offspring by varying allocation to eggs and embryos. Allocation may be adaptive based on the environmental conditions perceived during early breeding. We investigated the effects of food supplementation and predation risk on yolk hormone transfer in the pied flycatcher Ficedula hypoleuca. In a food supplementation experiment, females were food‐supplemented prior to and during egg‐laying and androgen concentrations were measured throughout the laying order. Predation risk was investigated in three different studies combining both correlative data, where flycatchers bred in close proximity to two different predator species that prey upon adult flycatchers (either Tengmalm's owl Aegolius funereus or pygmy owl Glaucidium passerinum), and an experimental manipulation, where flycatchers were exposed to cues of a nest predator (least weasel Mustela nivalis). Females receiving food supplementation laid eggs with lower concentrations of androstenedione (A4) than females not receiving food supplements. Yolk testosterone (T) concentration showed the same pattern but the difference was not statically significant. Testosterone (but not A4) concentration increased within clutches, from the first to the last egg, independently of the food supplementation. Females breeding under high predation risk did not differ from control females in their yolk androgen levels (A4, T or progesterone). However, concentrations of A4 tended to be lower in the proximity of pygmy owls, which could indirectly increase offspring survival after fledging. Food supplementation during egg‐laying seems to have a stronger impact on maternal transfer of androgens than predation risk. Food availability and predation risk could differentially affect the trade‐offs of androgen allocation for the offspring when raised in good vs. dangerous environments.

Experimental manipulation of food availability leads to short‐term intra‐clutch adjustment in egg mass but not in yolk androgen or thyroid hormones

In birds, mothers can affect their offspring's phenotype and thereby survival via egg composition. It is not well known to what extent and time‐scales environmental variation in resource availability, either via resource constrains or adaptive adjustment to predicted rearing conditions, influences maternal effects. We experimentally studied whether egg and yolk mass and yolk hormone levels respond to short‐term changes in food availability during laying in wild great titsParus major. Our treatment groups were: 1) food supplementation (mealworms) from the 1st until the last egg; 2) food supplementation from the 1st until the 5th egg, where the effect of cessation of the supplementary food treatment could also be studied; 3) no food supplementation (controls). We analysed both nutritional resources (egg, yolk and albumen mass), and the important developmental signals, yolk androgens (testosterone and androstenedione), and for the first time in a wild population, yolk thyroid hormones (thyroxine and 3,5,3′‐triiodothyronine). Egg mass is a costly resource for females, androgens most likely non‐costly signals, whereas thyroid hormones may be costly signals, requiring environmental iodine. In the food supplemented group egg, yolk and albumen mass increased rapidly relative to controls and when food supplementation was halted, egg and albumen mass decreased, indicating rapid responses to resource availability. Yolk androgen and thyroid hormone levels were not affected by food supplementation during laying. Thyroxine showed an increase over the laying sequence and its biological meaning needs further study. The rapid changes in egg mass to variation in within‐clutch food availability suggest energetic/protein/nutrient constrains on egg formation. The lack of a response in yolk hormones suggest that perhaps in this species the short‐term changes in resource availability during egg laying do not predict offspring rearing conditions, or (for thyroid hormones) do not cause systemic changes in circulating hormones, and hence do not affect maternal signaling.

Differential Effects of Maternal Yolk Androgens on Male and Female Offspring: A Role for Sex-Specific Selection?

Maternal hormones are important mediators of prenatal maternal effects in animals. Although their effects on offspring phenotype are often sex-specific, the reason why sometimes sons are more sensitive to prenatal hormone exposure and sometimes daughters is not well understood. Here I combine an experimental manipulation of yolk testosterone concentration in the egg and quantification of selection acting on yolk androgen-sensitive traits in a natural population of great tits (Parus major) with a literature review to test the hypothesis that sex-specific selection on traits affected by yolk androgens determines which sex is more sensitive to prenatal hormone exposure. An experimental increase of the testosterone content in the egg boosted the post-hatching growth of male, but not female great tit nestlings. However, I found no evidence that survival selection on body mass or size is acting differently in the two sexes. A literature review revealed that yolk androgen manipulations affect the growth of males and females differently across species. Interestingly, in studies performed in the wild a significant association between the strength and direction of sexual size dimorphism and sex-specific sensitivities to yolk androgens was observed. In studies performed in captivity, no such relationship was found. Thus, across species there is some evidence that sex-specific selection on body size influences how strongly growth trajectories of males and females are affected by maternally-derived yolk androgens.

Context-dependent effects of yolk androgens on nestling growth and immune function in a multibrooded passerine.

Female birds may adjust their offspring phenotype to the specific requirements of the environment by differential allocation of physiologically active substances into yolks, such as androgens. Yolk androgens have been shown to accelerate embryonic development, growth rate and competitive ability of nestlings, but they can also entail immunological costs. The balance between costs and benefits of androgen allocation is expected to depend on nestling environment. We tested this hypothesis in a multibrooded passerine, the spotless starling, Sturnus unicolor. We experimentally manipulated yolk androgen levels using a between-brood design and evaluated its effects on nestling development, survival and immune function. Both in first and replacement broods, the embryonic development period was shorter for androgen-treated chicks than controls, but there were no differences in second broods. In replacement broods, androgen-treated chicks were heavier and larger than those hatched from control eggs, but this effect was not observed in the other breeding attempts. Androgen exposure reduced survival with respect to controls only in second broods. Regarding immune function, we detected nonsignificant trends for androgen treatment to activate two important components of innate and adaptive immunity (IL-6 and Ig-A levels, respectively). Similarly, androgen-treated chicks showed greater lymphocyte proliferation than controls in the first brood and an opposite trend in the second brood. Our results indicate that yolk androgen effects on nestling development and immunity depend on the environmental conditions of each breeding attempt. Variation in maternal androgen allocation to eggs could be explained as the result of context-dependent optimal strategies to maximize offspring fitness.