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In colonial breeding species, the number of adverse social interactions during early life typically varies with breeding density. Phenotypic plasticity can help deal with this social context, by allowing offspring to adjust their behaviour. Furthermore, offspring may not be unprepared since mothers can allocate resources to their embryos that may pre-adjust them to the post-hatching conditions. Thus, we hypothesize that lesser black-backed gull chicks raised in dense breeding areas, with greater exposure to intra-specific aggression, show higher levels of anxiety and lower levels of exploration compared to chicks in low-density areas, and that this is facilitated by prenatal effects. To test this, we cross-fostered clutches within and across pre-defined high- and low-breeding density areas. We measured chicks' anxiety and exploration activity in an open-field test that included a novel and a familiar object. We found that both pre- and post-natal social environment contributed nearly equally and shaped the offspring's exploratory behaviour, but not its anxiety, in an additive way. Post-natal effects could reflect a learned avoidance of intra-specific aggression, yet identifying the pathways of the prenatal effects will require further study.

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 tits (Parus major). Our treatment groups were: 1) food supplementation (mealworms) from the 1st until the last egg; 2) food supplementation from the 1st first 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.

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. (C) 2012 Elsevier Inc. All rights reserved.

In birds, early exposure to androgens has been shown to influence offspring growth and begging behaviour, and has been proposed as a mechanism for the development of sexual size dimorphism (SSD). Sex specific effects during development can occur due to sex-specific allocation of maternal androgens, sensitivity to, or synthesis of, androgens. In addition, maternal hormones have been suggested as a mechanism to skew brood sex ratio. This study uses one of the world's most extreme SSD species, the brown songlark Cinclorhamphus cruralis, to investigate (1) sex-specific differences of androgens in yolk and chick plasma and (2) the relationship between androgens and sex ratio bias. The study reveals no indication of sex-specific maternal allocation, but a modest sex effect during the later stages of incubation when the embryo starts to produce its own androgens. Moreover, there was a strong seasonal sex ratio bias: female-biased early and male-biased later in the season, but yolk testosterone (T) did not show a seasonal trend. Taken together these results suggest that if androgens, from any source, have a significant role in development of SSD in this species it is most likely via sex-specific sensitivity or synthesis rather than differential maternal transfer to the egg. (C) 2009 Elsevier Inc. All rights reserved.

Mates and females are in conflict over parental care, as it would be favourable for one parent to shift labour to the other. Yolk hormones may offer a mechanism through which female birds could influence offspring traits in ways that increase the relative investment by the male. We studied the role of yolk androgens in mediating sexual conflict over parental care in the collared flycatcher (Ficedula albicollis). In a cross-fostering experiment, the male's proportion of total feeding visits increased with increasing androgen levels in the foster eggs. This could suggest that sexual conflict over parental care may be influenced by the female's differential allocation of yolk androgens or a maternal effect associated with yolk androgens. However, when we experimentally elevated yolk androgen levels, male feeding rates did not differ between control and androgen-manipulated nests. This suggests that other egg components correlated with yolk androgen levels, rather than yolk androgen levels per se, may influence male parental effort. In conclusion, yolk androgens per se do not appear to mediate sexual conflict over parental investment in the collared flycatcher. (C) 2009 Elsevier Inc. All rights reserved.

Maternal hormones in vertebrate eggs can mediate important forms of maternal effects. However, the function of hormone transfer to the eggs is still debated, especially because long-term fitness consequences have been little studied. We investigated the effect of prenatal exposure to physiologically elevated yolk testosterone (T) levels on reproduction of female pheasants ( Phasianus colchicus ) in captivity. We found that females hatching from T-injected eggs (T-females) had a lower egg-laying rate than controls, and their eggs were more frequently infertile than those laid by control females. There were no effects of prenatal maternal treatment on egg size and yolk T concentration, but eggs carrying a female embryo laid by T-females had smaller yolks than eggs with a male embryo, while there was no sex difference in yolk size among the eggs laid by control females. Progeny sex ratio was unaffected by maternal treatment. These findings suggest that the transfer of high androgen levels to the eggs by the mother is constrained by complex trade-offs between direct effects on her daughters’ reproduction and by trans-generational differential consequences on male and female descendants.

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation.Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.

Abstract Based on Tinbergen's view of the study of behavioural development we describe some recent advances and their importance in this field. We argue that the study of behavioural development should combine both proximate and ultimate approaches, and can help to understand how early subtle environmental factors shape consistent individual variation both between and within sexes. This is illustrated by reviewing the profound effects of incubation temperature on the development of brain and social behaviour in the leopard gecko, a species with temperature-dependent sex determination, and the effects of early exposure to steroid hormones on social behaviour in rodents and especially birds. Both are maternal effects: incubation temperature can be partly determined by the nest site where the mother deposited her eggs, while in both oviparous and viviparous vertebrates maternal hormones reach and influence the embryo. In the gecko, incubation temperature affects sexual and aggressive behaviour, growth, the hypothalamus-pituitary-gonadal axis, as well as the size, connectivity and metabolic capacity of certain brain areas. In this way not only is the gonad type determined, but so too is the morphological, physiological, neural, and behavioural phenotype established that explains much of within-sex variation. In rodents, maternal hormones affect similar aspects. In avian species, maternal hormones, deposited in the eggs, vary systematically between and within clutches and have both short- and long-lasting effects on competitive behaviour. Evidence suggests that mothers adaptively adjust hormone allocation to the environmental context. In addition, we discuss some effects of postnatal experience on behavioural development in geckos, mice and bird species. Our results also illustrate how the study of animal models other than rodents can help in understanding important developmental processes.

Avian eggs contain considerable amounts of maternal yolk androgens, which have been shown to beneficially influence the physiology and behaviour of the chick. As androgens may suppress immune functions, they may also entail costs for the chick. This is particularly relevant for colonial species, such as the black-headed gull (Larus ridibundus), in which the aggregation of large numbers of birds during the breeding season enhances the risk of infectious diseases for the hatching chick.To test the effect of maternal yolk androgens on the chick's immune function, we experimentally manipulated, in a field study, yolk androgen levels within the physiological range by in ovo injection of either androgens (testosterone and androstenedione) or sesame oil (control) into freshly laid eggs. We determined cell-mediated immunity (CMI) and humoral immunity of the chicks at the beginning of the nestling period to evaluate early modulatory effects of yolk androgens on immune function.Embryonic exposure to elevated levels of androgens negatively affected both CMI and humoral immunity in nestling gull chicks. Consequently, maternal yolk androgens not only entail benefits of enhanced competitiveness and growth as previously shown, but also costs in terms of immunosuppression. The outcome of embryonic yolk androgen exposure thus likely depends on the post-hatching circumstances for the developing offspring such as parasite exposure and degree of sibling competition.

Avian eggs contain substantial levels of various hormones of maternal origin and have recently received a lot of interest, mainly from behavioral ecologists. These studies strongly depend on the measurement of egg hormone levels, but the method of measuring these levels has received little attention. This paper describes the sampling, extraction, and assay of hormones in avian eggs and related methodological problems. The method of sampling is important because hormones are not homogeneously distributed within the egg, and after onset of embryonic development their levels may decrease and increase due to changes in egg structure and secretion or uptake of hormones by the embryo. The extraction of hormones from the yolk and chromatographic separation of different hormones for immunoassays can strongly influence the results because such procedures remove interfering substances such as proteins, lipids, and other hormones and their metabolites, which can cross-react with the antiserum used. Finally, the assay itself needs more validation than many studies report, especially with respect to the accuracy and specificity of the hormone measurements. We conclude that the addressed issues need more attention for the correct interpretation of differences in hormone levels within and between studies.

Black-headed gulls, Larus ridibundus, produce clutches of three eggs, which contain high levels of maternal androgens in the yolk. These levels increase with laying order and the eggs hatch asynchronously. Experiments have supported the hypothesis that this within-clutch variation in maternal androgens mitigates the disadvantage of last-hatched chicks in sibling competition, by enhancing embryonic development and early posthatching growth. We hypothesized that these effects come about by the stimulating effects of maternal androgens on begging behaviour and competitive ability. In the field, we injected first-laid eggs of a clutch (which have a low androgen level) with either an androgen solution (T eggs) or vehicle (Oil eggs). We then created pairs of chicks hatched from Oil and T eggs, matched for egg mass and hatching date. Parent-chick interactions were recorded from observation hides. Chicks from T eggs hatched almost half a day sooner than those from Oil eggs. Furthermore, chicks from T eggs were more active during the first week after hatching, were more often the first to react to the approaching parent, begged more frequently, and obtained the larger share of food. We conclude that the enhancing effect of yolk androgens on growth in this species arises at least partly through androgen-mediated effects on the chicks' behaviour. (C) 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Hatching asynchrony in avian species leads to age and size differences between nestlings within a brood, handicapping last-hatched chicks in the sibling rivalry. Starvation due to this competitive disadvantage has been regarded as the primary cause of an increase in mortality with hatching order. However, for gulls it has also been suggested that disease is the cause of mortality for last-hatched chicks, possibly through reduced immunocompetence and thereby an enhanced susceptibility to infection. In addition, the male-biased mortality reported for several gull species may be related to a higher vulnerability to diseases in males compared to females. To determine the potential influence of the immune system on these mortality patterns, we investigated the T-cell-mediated immunity (CMI) of black-headed gull chicks in relation to hatching order and sex. We found a significant decrease in the CMI with hatching order. This result may be causally related to systematic changes in maternal yolk steroids and carotenoids within the laying sequence. For second-laid eggs, male CMI was significantly lower than female CMI. This is possibly linked to higher plasma levels of testosterone in male embryos which might have an immunosuppressive effect. If so, this effect is masked in eggs of either high (first egg) or low (last egg) quality. Chicks with low CMI showed enhanced mortality rates. Thus the differences in immune response are likely to contribute to the observed mortality patterns. However, hatching order significantly affected mortality independently of CMI, suggesting that competitive disadvantage due to hatching asynchrony is also important.

We tested the challenge hypothesis for the hormonal regulation of aggression in chicks of the black-headed gull, Larus ridibundus. Chicks of this species are highly aggressive toward conspecifics, but never to peers that hatched from the same clutch (modal clutch size is three). Therefore, in the first experiment small families were housed together in large groups (challenged condition) and compared to families kept isolated (nonchallenged condition). As expected, in the challenged condition during the initial stage of territory establishment basal levels of testosterone M were clearly higher than those in the nonchallenged condition. In the second experiment we tested the effect of a short social challenge on short-term T-fluctuations. The design was based on an earlier experiment, showing that after temporary T-treatment chicks become very sensitive to social challenges while having low basal T-levels. We now show that these social challenges induce brief elevations in plasma T-levels. These peaks are similar to those in previously untreated chicks but untreated chicks do not respond with aggression to a challenge. Therefore, we conclude that the initial exposure to elevated T-levels increases the sensitivity to brief changes in T induced by social challenges. In this way exposure to T, that may be detrimental for development, is minimized while birds remain able to defend territories. This is the first report showing that the challenge hypothesis as established for adult birds, is also applicable for aggressive behavior in young birds outside the sexual context. Furthermore we suggest that a phase of priming with T is necessary to obtain the high behavioral responsiveness to a challenge. (C) 2002 Elsevier Science (USA).

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.

International audience; An animal's emotional responses are the result of its cognitive appraisal of a situation. This appraisal is notably influenced by the possibility of an individual to exert control over an aversive event. Although the fact that environment controllability decreases emotional responses in animals is well established, far less is known about its potential trans-generational effects. As the levels of avian yolk hormones can vary according to the mother's environment, we hypothesized that housing environment of mothers would modulate the quality of her eggs and in turn her offspring's behaviour. Two groups of female japanese quail were constituted: a group that had access to a place to hide in their home-cage (Hd, n = 20) and a group that had nowhere to hide (NoHd, n = 20) when stressed. Both groups were submitted to daily human disturbances for a twenty-day-period. Hd females produced eggs with both less testosterone and androstenedione than did NoHd females. The emotional and social reactivity of Hd female's offspring were lower and their growth wes slower than those of NoHd females' offspring. Our results show that a minor difference in housing environment had substantial effects on eggs and offspring. The presence of a shelter probably helped quail to cope with daily human disturbances, producing less reactive offspring. This transgenerational effect caused by an opportunity to hide could lead to applications in care of laboratory animals, conservation biology and animal welfare.

1. During early development male offspring in avian species often suffer from enhanced mortality compared to female offspring. This has been attributed to different nutritional requirements, as sex-biased mortality has been reported particularly in sexually sizedimorphic species. However, other traits of the male phenotype, such as the embryonic hormone profile, have been suggested to contribute to this male disadvantage. In particular the negative effects of sex steroids on immune function may be causally involved. 2. We investigated the role of testosterone in the expression of male phenotype disadvantage through an experimental reduction of the availability of testosterone receptors by in-ovo injection of an anti-androgen (Flutamide©). Experimental nests contained a male and a female chick hatching from control treated eggs and a male and a female chick hatching from Flutamide treated eggs. 3. Male-biased mortality occurred in control chicks at a stage where the sexes did not yet differ in their growth pattern, suggesting that sex-specific nutritional requirements are not necessary for male-biased mortality to occur. Control males and control females did not differ in their cell-mediated immunity (CMI). This renders it unlikely that the observed skewed mortality was due to sex-specific differences in the CMI. 4. Treatment of the eggs with flutamide antagonistically affected males and females. Flutamide treatment positively affected male development in particular through an enhanced growth rate, indicating that testosterone is involved in the expression of the male phenotype disadvantage. Female chicks hatching from Flutamide treated eggs were disadvantaged in growth and CMI. The possible pathways of this sex-specific effect of Flutamide are discussed with regard to differential consequences of blocking the beneficial effects of maternal androgens and the interference with the process of sexual differentiation in males. Key-words : anti-androgen, brood

Dispersal is a major determinant of the dynamics and genetic structure of populations, and its consequences depend not only on average dispersal rates and distances, but also on the characteristics of dispersing and philopatric individuals. We investigated whether natal dispersal correlated with a predisposed behavioural trait: exploratory behaviour in novel environments. Wild great tits were caught in their natural habitat, tested the following morning in the laboratory using an open field test and released at the capture site. Natal dispersal correlated positively with parental and individual exploratory behaviour, using three independent datasets. First, fast-exploring parents had offspring that dispersed furthest. Second, immigrants were faster explorers than locally born birds. Third, post-fledging movements, comprising a major proportion of the variation in natal dispersal distances, were greater for fast females than for slow females. These findings suggest that parental behaviour influenced offspring natal dispersal either via parental behaviour per se (e.g. via post-fledging care) or by affecting the phenotype of their offspring (e.g. via their genes). Because this personality trait has a genetic basis, our results imply that genotypes differ in their dispersal distances. Therefore, the described patterns have profound consequences for the genetic composition of populations.