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.

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.

Measuring endogenous corticosterone in laboratory mice - a mapping review, meta-analysis, and open source database.

Evaluating stress in laboratory animals is a key principle in animal welfare. Measuring corticosterone is a common method to assess stress in laboratory mice. There are, however, numerous methods to measure glucocorticoids with differences in sample matrix (e.g., plasma, urine) and quantification techniques (e.g., enzyme immunoassay or radioimmunoassay). Here, the authors present a mapping review and a searchable database, giving a complete overview of all studies mea­suring endogenous corticosterone in mice up to February 2018. For each study, information was recorded regarding mouse strain and sex; corticosterone sample matrix and quantification technique; and whether the study covered the research theme animal welfare, neuroscience, stress, inflammation, or pain (the themes of specific interest in our con­sortium). Using all database entries for the year 2012, an exploratory meta-regression was performed to determine the effect of predictors on basal corticosterone concentrations. Seventy-five studies were included using the predictors sex, time-since-lights-on, sample matrix, quantification technique, age of the mice, and type of control. Sex, time-since-lights-on, and type of control significantly affected basal corticosterone concentrations. The resulting database can be used, inter alia, for preventing unnecessary duplication of experiments, identifying knowledge gaps, and standardizing or heterogenizing methodologies. These results will help plan more efficient and valid experiments in the future and can answer new questions in silico using meta-analyses.

Importance of Basic Research on the Causes of Feather Pecking in Relation to Welfare.

Feather pecking is a prominent issue in the commercial egg industry, associated with economic losses and welfare problems. A non-systematic literature search suggests that studies on feather pecking are predominantly concerned with applied research goals. That is to say, they aim to solve or diminish the effects of this problematic behavior by orienting towards practical approaches. The strong emphasis on this research approach has skewed our knowledge of the causes of feather pecking in relation to welfare. While the need for such research is high, there is an equivalent need for basic research that has not received corresponding effort. Also, current research predominantly focuses on the negative effects on the birds being pecked, whereas too little attention is given to the possible welfare problems of the peckers. We argue that more basic research is needed for obtaining comprehensive science-based knowledge of behavioral needs and abilities of hens, in particular with respect to behavioral problems that threaten their welfare.

Measurement of corticosterone in mice: a protocol for a mapping review.

Severity assessment for experiments conducted with laboratory animals is still based mainly on subjective evaluations; evidence-based methods are scarce. Objective measures, amongst which determination of the concentrations of stress hormones, can be used to aid severity assessment. Short-term increases in glucocorticoid concentrations generally reflect healthy responses to stressors, but prolonged increases may indicate impaired welfare. As mice are the most commonly used laboratory animal species, we performed a systematic mapping review of corticosterone measurements in Mus musculus, to provide a full overview of specimen types (e.g. blood, urine, hair, saliva, and milk) and analysis techniques. In this publication, we share our protocol and search strategy, and our rationale for performing this systematic analysis to advance severity assessment. So far, we have screened 13,520 references, and included 5337 on primary studies with measurements of endogenous corticosterone in M. musculus. Data extraction is currently in progress. When finished, this mapping review will be a valuable resource for scientists interested in corticosterone measurements to aid severity assessment. We plan to present the data in a publication and a searchable database, which will allow for even easier retrieval of the relevant literature. These resources will aid implementation of objective measures into severity assessment.

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.].

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.

Early stress causes sex-specific, life-long changes in behaviour, levels of gonadal hormones, and gene expression in chickens.

Early stress can have long-lasting phenotypic effects. Previous research shows that male and female chickens differ in many behavioural aspects, and respond differently to chronic stress. The present experiment aimed to broadly characterize long-term sex differences in responses to brief events of stress experienced during the first weeks of life. Chicks from a commercial egg-laying hybrid were exposed to stress by inducing periods of social isolation during their first three weeks of life, followed by a broad behavioural, physiological and genomic characterization throughout life. Early stressed males, but not females, where more anxious in an open field-test, stayed shorter in tonic immobility and tended to have delayed sexual maturity, as shown by a tendency for lower levels of testosterone compared to controls. While early stressed females did not differ from non-stressed in fear and sexual maturation, they were more socially dominant than controls. The differential gene expression profile in hypothalamus was significantly correlated from 28 to 213 days of age in males, but not in females. In conclusion, early stress had a more pronounced long-term effect on male than on female chickens, as evidenced by behavioral, endocrine and genomic responses. This may either be attributed to inherent sex differences due to evolutionary causes, or possibly to different stress related selection pressures on the two sexes during commercial chicken breeding.

Manipulation of primary sex ratio in birds: lessons from the homing pigeon (Columba livia domestica).

Across various animal taxa not only the secondary sex ratio but also the primary sex ratio (at conception) shows significant deviations from the expected equal proportions of sons and daughters. Birds are especially intriguing to study this phenomenon as avian females are the heterogametic sex (ZW); therefore sex determination might be under direct control of the mother. Avian sex ratios vary in relation to environmental or maternal condition, which can also affect the production of maternal steroids that in turn are involved in reproduction and accumulate in the developing follicle before meiosis. As the proximate mechanisms underlying biased primary sex ratio are largely elusive, we explored how, and to what extent, maternal steroid hormones may be involved in affecting primary or secondary sex ratio in clutches of various species of pigeons. First we demonstrated a clear case of seasonal change in sex ratio in first eggs both in the Rock Pigeon (Columba livia) and in a related species, the Wood Pigeon (Columba palumbus), both producing clutches of two eggs. In the Homing Pigeon (Columba livia domestica), domesticated from the Rock Pigeon, testosterone treatment of breeding females induced a clear male bias, while corticosterone induced a female bias in first eggs and we argue that this is in line with sex allocation theory. We next analyzed treatment effects on follicle formation, yolk mass, and yolk hormones, the latter both pre- and post-ovulatory, in order to test a diversity of potential mechanisms related to both primary and secondary sex ratio manipulation. We conclude that maternal plasma hormone levels may affect several pre-ovulatory mechanisms affecting primary sex ratio, whereas egg hormones are probably involved in secondary sex ratio manipulation only.