Effects of the maternal and current social environment on female body mass and reproductive traits in Japanese quail (Coturnix japonica).

The social environment of breeding females can affect their phenotype, with potential adaptive maternal effects on offspring that experience a similar environment. We housed Japanese quail (Coturnix japonica) females in two group sizes (pairs versus groups of four) and studied the effects on their offspring under matched and mismatched conditions. We measured F1 body mass, reproduction, and plasma levels of androgens and corticosterone. F1 group housing led to an increase in body mass. In addition, F1 group housing had a positive effect on mass in daughters of pair-housed P0 females only, which were heaviest under mismatched conditions. At the time of egg collection for the F2 generation, F1 group-housed females were heavier, irrespective of the P0 treatment. F1 females in groups laid heavier eggs, with higher hatching success, and produced heavier offspring, most likely a maternal effect of F1 mass. F1 plasma hormones were affected by neither the P0 nor the F1 social environment. These results contrasted with effects in the P0 generation (reported previously), in which plasma hormone levels, but not mass, differed between social environments. This may be due to changes in adult sex ratios as P0 females were housed with males, whereas F1 females encountered males only during mating. Our study demonstrates potentially relevant mismatch effects of the social environment on F1 body mass and maternal effects on F2 offspring, but further study is needed to understand their adaptive significance and physiological mechanisms.

Correction: Social environment during egg laying: Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica.

[This corrects the article DOI: 10.1371/journal.pone.0176146.].

No evidence for sex-specific effects of the maternal social environment on offspring development in Japanese quail (Coturnix japonica).

The social environment of reproducing females can cause physiological changes, with consequences for reproductive investment and offspring development. These prenatal maternal effects are often found to be sex-specific and may have evolved as adaptations, maximizing fitness of male and female offspring for their future environment. Female hormone levels during reproduction are considered a potential mechanism regulating sex allocation in vertebrates: high maternal androgens have repeatedly been linked to increased investment in sons, whereas high glucocorticoid levels are usually related to increased investment in daughters. However, results are not consistent across studies and therefore still inconclusive. In Japanese quail (Coturnix japonica), we previously found that pair-housed females had higher plasma androgen levels and tended to have higher plasma corticosterone levels than group-housed females. In the current study we investigate whether these differences in maternal social environment and physiology affect offspring sex allocation and physiology. Counter to our expectations, we find no effects of the maternal social environment on offspring sex ratio, sex-specific mortality, growth, circulating androgen or corticosterone levels. Also, maternal corticosterone or androgen levels do not correlate with offspring sex ratio or mortality. The social environment during reproduction therefore does not necessarily modify sex allocation and offspring physiology, even if it causes differences in maternal physiology. We propose that maternal effects of the social environment strongly depend upon the type of social stimuli and the timing of changes in the social environment and hormones with respect to the reproductive cycle and meiosis.

Social environment during egg laying: Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica.

The social environment can have profound effects on an individual's physiology and behaviour and on the transfer of resources to the next generation, with potential consequences for fecundity and reproduction. However, few studies investigate all of these aspects at once. The present study housed female Japanese quail (Coturnix japonica) in pairs or groups to examine the effects on hormone concentrations in plasma and yolk and on reproductive performance. Circulating levels of androgens (testosterone and 5-α-dihydrotestosterone) and corticosterone were measured in baseline samples and after standardised challenges to assess the responsiveness of the females' endocrine axes. Effects of the social environment on female fecundity were analysed by measuring egg production, egg mass, fertilization rates, and number of hatched offspring. Counter to expectation, females housed in pairs had higher plasma androgen concentrations and slightly higher corticosterone concentrations than females housed in groups, although the latter was not statistically significant. Pair vs. group housing did not affect the females' hormonal response to standardised challenges or yolk testosterone levels. In contrast to previous studies, the females' androgen response to a gonadotropin-releasing hormone challenge was not related to yolk testosterone levels. Non-significant trends emerged for pair-housed females to have higher egg-laying rates and higher fertility, but no differences arose in egg weight or in the number, weight or size of hatchlings. We propose that our unexpected findings are due to differences in the adult sex ratio in our social treatments. In pairs, the male may stimulate female circulating hormone levels more strongly than in groups where effects are diluted due to the presence of several females. Future studies should vary both group size and sex composition to disentangle the significance of sexual, competitive and affiliative social interactions for circulating and yolk hormone levels, and their consequences for subsequent generations.

Effects of the social environment during adolescence on the development of social behaviour, hormones and morphology in male zebra finches (Taeniopygia guttata).

BACKGROUND: Individual differences in behaviour are widespread in the animal kingdom and often influenced by the size or composition of the social group during early development. In many vertebrates the effects of social interactions early in life on adult behaviour are mediated by changes in maturation and physiology. Specifically, increases in androgens and glucocorticoids in response to social stimulation seem to play a prominent role in shaping behaviour during development. In addition to the prenatal and early postnatal phase, adolescence has more recently been identified as an important period during which adult behaviour and physiology are shaped by the social environment, which so far has been studied mostly in mammals. We raised zebra finches (Taeniopygia guttata) under three environmental conditions differing in social complexity during adolescence - juvenile pairs, juvenile groups, and mixed-age groups - and studied males' behavioural, endocrine, and morphological maturation, and later their adult behaviour. RESULTS: As expected, group-housed males exhibited higher frequencies of social interactions. Group housing also enhanced song during adolescence, plumage development, and the frequency and intensity of adult courtship and aggression. Some traits, however, were affected more in juvenile groups and others in mixed-age groups. Furthermore, a testosterone peak during late adolescence was suppressed in groups with adults. In contrast, corticosterone concentrations did not differ between rearing environments. Unexpectedly, adult courtship in a test situation was lowest in pair-reared males and aggression depended upon the treatment of the opponent with highest rates shown by group-reared males towards pair-reared males. This contrasts with previous findings, possibly due to differences in photoperiod and the acoustic environment. CONCLUSION: Our results support the idea that effects of the adolescent social environment on adult behaviour in vertebrates are mediated by changes in social interactions affecting behavioural and morphological maturation. We found no evidence that long-lasting differences in behaviour reflect testosterone or corticosterone levels during adolescence, although differences between juvenile and mixed-age groups suggest that testosterone and song behaviour during late adolescence may be associated.

Offspring Hormones Reflect the Maternal Prenatal Social Environment: Potential for Foetal Programming?

Females of many species adaptively program their offspring to predictable environmental conditions, a process that is often mediated by hormones. Laboratory studies have shown, for instance, that social density affects levels of maternal cortisol and testosterone, leading to fitness-relevant changes in offspring physiology and behaviour. However, the effects of social density remain poorly understood in natural populations due to the difficulty of disentangling confounding influences such as climatic variation and food availability. Colonially breeding marine mammals offer a unique opportunity to study maternal effects in response to variable colony densities under similar ecological conditions. We therefore quantified maternal and offspring hormone levels in 84 Antarctic fur seals (Arctocephalus gazella) from two closely neighbouring colonies of contrasting density. Hair samples were used as they integrate hormone levels over several weeks or months and therefore represent in utero conditions during foetal development. We found significantly higher levels of cortisol and testosterone (both P < 0.001) in mothers from the high density colony, reflecting a more stressful and competitive environment. In addition, offspring testosterone showed a significant positive correlation with maternal cortisol (P < 0.05). Although further work is needed to elucidate the potential consequences for offspring fitness, these findings raise the intriguing possibility that adaptive foetal programming might occur in fur seals in response to the maternal social environment. They also lend support to the idea that hormonally mediated maternal effects may depend more strongly on the maternal regulation of androgen rather than cortisol levels.

The maternal social environment shapes offspring growth, physiology, and behavioural phenotype in guinea pigs.

BACKGROUND: Prenatal conditions influence offspring development in many species. In mammals, the effects of social density have traditionally been considered a detrimental form of maternal stress. Now their potential adaptive significance is receiving greater attention.Sex-specific effects of maternal social instability on offspring in guinea pigs (Cavia aperea f. porcellus) have been interpreted as adaptations to high social densities, while the effects of low social density are unknown. Hence, we compared morphological, behavioural and physiological development between offspring born to mothers housed either individually or in groups during the second half of pregnancy. RESULTS: Females housed individually and females housed in groups gave birth to litters of similar size and sex-ratios, and there were no differences in birth weight. Sons of individually-housed mothers grew faster than their sisters, whereas daughters ofgroup-housed females grew faster than their brothers, primarily due to an effect on growth of daughters. There were few effects on offspring behaviour. Baseline cortisol levels in saliva of pups on day 1 and day 7 were not affected, but we saw a blunted cortisol response to social separation on day 7 in sons of individually-housed females and daughters of group-housed females. The effects were consistent across two replicate experiments. CONCLUSIONS: The observed effects only partially support the adaptive hypothesis. Increased growth of daughters may be adaptive under high densities due to increasedfemale competition, but it is unclear why growth of sons is not increased under low social densities when males face less competition from older, dominant males. The differences in growth may be causally linked to sex-specific effects on cortisol response, although individual cortisol response and growth were not correlated, and various other mechanisms are possible. The observed sex-specific effects on early development are intriguing, yet the potential adaptive benefits and physiological mechanisms require further study.

Effects of social conditions during adolescence on courtship and aggressive behavior are not abolished by adult social experience.

Social experience during adolescence has long-lasting consequences for adult social behavior in many species. In zebra finches, individuals reared in pairs during adolescence start to court females faster, sing more courtship motifs to females and are more aggressive compared with group-reared males. We investigated whether such differences are stable during adulthood or can be abolished by novel social experience after adolescence by giving all birds extensive experience with group life during adulthood. Courtship and aggressiveness increased in all males, but pair-reared males still had a higher motif rate and were more aggressive than group-reared males. Males no longer differed in courtship latency. In addition to the stable treatment differences, individual differences in behavior remained stable over time. Our results show that differences in behavior acquired during adolescence are preserved into adulthood, although adults still change their social behavior. Adolescence can thus be seen as a sensitive period during which social conditions have a lasting effect on adult behavior.

Collective cognition in humans: groups outperform their best members in a sentence reconstruction task.

Group-living is widespread among animals and one of the major advantages of group-living is the ability of groups to solve cognitive problems that exceed individual ability. Humans also make use of collective cognition and have simultaneously developed a highly complex language to exchange information. Here we investigated collective cognition of human groups regarding language use in a realistic situation. Individuals listened to a public announcement and had to reconstruct the sentence alone or in groups. This situation is often encountered by humans, for instance at train stations or airports. Using recent developments in machine speech recognition, we analysed how well individuals and groups reconstructed the sentences from a syntactic (i.e., the number of errors) and semantic (i.e., the quality of the retrieved information) perspective. We show that groups perform better both on a syntactic and semantic level than even their best members. Groups made fewer errors and were able to retrieve more information when reconstructing the sentences, outcompeting even their best group members. Our study takes collective cognition studies to the more complex level of language use in humans.

Early social instability affects plasma testosterone during adolescence but does not alter reproductive capacity or measures of stress later in life.

The social environment plays an important role in modulating processes of the hormonal and behavioural profile of an animal in a variety of group-living species. In wild cavies for instance, unstable social environmental conditions during pregnancy and lactation lead to an infantilised biobehavioural profile of the male offspring. In the present study, the influence of the social environment during pregnancy and lactation on the male wild cavy offsprings' plasma testosterone development, reproductive capacity and stress system activity was investigated. To this purpose, 12 sons whose mothers had lived in an unstable social environment during pregnancy and lactation were compared with 12 sons whose mothers had lived in a stable social environment during the same time. Plasma testosterone (T) and plasma cortisol (C) concentrations were determined from days 20 to 107 of age. Adrenal tyrosine hydroxylase (TH) activity and different parameters of reproductive capacity (weights of testes, epididymides and accessory sex glands, cellular composition of the testes, DNA fragmentation indices and sperm motility parameters) were analysed at day 107 of age. TH activity and plasma C were unaffected by different social environmental conditions early in life. The developmental time course of T concentrations, however, was significantly different: Sons whose mothers had lived in an unstable social environment during pregnancy and lactation showed a delayed increase in T concentrations around adolescence compared to controls. In contrast, no reproduction-related parameters measured within this study differed significantly between the two groups. Thus, early social instability affects plasma testosterone development during adolescence in a significant way but does not alter reproductive capacity or measures of stress later in life.

Differential maternal testosterone allocation among siblings benefits both mother and offspring in the zebra finch Taeniopygia guttata.

Parents are selected to preferentially invest in the offspring with highest reproductive value. One mechanism for achieving this is the modification of competitive asymmetries between siblings by maternal hormones. In many organisms, offspring value varies according to birth position in the brood, which determines survival chances and competitive advantage over access to resources. In birds, variation in yolk androgen allocation over the laying sequence is thought to modulate dominance of senior chicks over junior brood mates. We tested this hypothesis in zebra finches, which show a naturally decreasing pattern of within-clutch testosterone allocation. We abolished these within-clutch differences by experimentally elevating yolk testosterone levels in eggs 2-6 to the level of egg 1, and we assessed fitness measures for junior offspring (eggs 2-6), senior offspring (egg 1), and their mothers. Testosterone-injected eggs hatched later than control eggs. Junior, but not senior, chicks in testosterone-treated broods attained poorer phenotypic quality compared to control broods, which was not compensated for by positive effects on seniors. Mothers were generally unaffected by clutch treatment. Thus, naturally decreasing within-clutch yolk testosterone allocation appears to benefit all family members and does not generally enhance brood reduction by favoring senior chicks, in contrast to the widely held assumption.

Steroids in chicken egg yolk: metabolism and uptake during early embryonic development.

Effects of maternal hormones may adaptively adjust offspring development to prevailing conditions. However, Darwinian fitness of parents is maximized by investing in more than one offspring while each individual offspring benefits from receiving maximal investment. The control of mother and offspring over hormone-mediated maternal effects is thought to play a key role in the outcome of parent-offspring conflict, but these control mechanisms have hardly been studied. We investigated the potential embryonic control by analysing the changes in distribution and metabolism of steroid hormones in the egg during the first 6 days of incubation using injections of radiolabelled testosterone and corticosterone in freshly laid eggs. After 1 day of incubation the highest amount of radioactivity was concentrated in a small area at the top of the yolk. This challenges the use of hormones in oil as mimicking natural exposure. During incubation radioactivity spread within the egg with highest concentrations in yolk and yolk sac and lower concentrations in albumen, embryo, allantois, and amnion. Steroids were metabolised to other unconjugated and conjugated steroids, perhaps facilitating embryonic steroid uptake. Our study shows that the injected radiolabel is metabolised in the egg and taken up by the embryo, giving the embryo potential control over the effects of maternal hormones and thereby limiting maternal control over the outcome of hormone-mediated maternal effects.

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.

Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus).

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.

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches.

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.

Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation.

The last decade has witnessed a surge in studies on steroid hormones of maternal origin present in avian eggs and affecting offspring development. The value of such studies for the understanding of maternal effects and individual differentiation is endorsed and a series of methodological and conceptual issues in the current approaches is discussed. First to be addressed is the topic of correct sampling of eggs or yolk for hormone analyses. Changes in yolk hormone levels during the incubation period and the uneven distribution of hormones within the egg are discussed. Different ways of calculating hormone levels and the importance of collecting data for specific a priori hypotheses are explained. Next to be discussed are the pros and cons of different techniques for manipulating yolk hormone levels and their proper scaling to naturally occurring levels. Third, several issues hampering the interpretation of results from descriptive and experimental studies are addressed. These concern biased embryonic mortality, clutch size, and egg quality that may confound the interpretation of the effect of egg position in the laying order, and the possibility of sex-specific effects and long-term effects. Also discussed are the probability of context-dependent results (due to, e.g., other egg components affecting egg quality, parental quality, and environmental factors), the difficulty in demonstrating adaptive effects due to individual optimization, and the lack of insight in the underlying physiological processes. Finally, it is concluded that this field has shown much progress but that it would profit from a more careful consideration of methodology and from a better integration of behavioral ecology and endocrinology.

Measuring steroid hormones in avian eggs.

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.

Maternal hormones as a tool to adjust offspring phenotype in avian species.

Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.

Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival.

Treatment of female zebra finches (Taeniopygia guttata) with 17-beta-estradiol leads to a female-biased sex ratio in their offspring at the age of independence [Horm. Behav. 35 (1999) 135]. It is unclear whether this is due to a bias of the primary sex ratio or to sex-specific survival. We replicated this experiment and found again a significantly higher total number of daughters than sons at independence in the estradiol-treated group. This was due to higher embryonic survival of daughters compared with sons in the estradiol-treated group and the reverse in the control group. There was no effect of the hormone treatment on the primary sex ratio. Treatment with 17-beta-estradiol led to a significantly shorter hatching time and to heavier offspring at day 7 after hatching. This weight was correlated with maternal plasma estradiol levels on the day of the first egg, which were significantly higher in the estradiol-treated group than in the control group. The results do not support the idea that maternal estradiol levels influence the primary sex ratio. They indicate that maternal estradiol differentially affects survival of sons and daughters via an influence on the embryonic environment, possibly enhancing offspring growth.