Maternal effects in the highly communal sociable weaver may exacerbate brood reduction and prepare offspring for a competitive social environment.

Maternal effects can influence offspring phenotype with short- and long-term consequences. Yet, how the social environment may influence egg composition is not well understood. Here, we investigate how laying order and social environment predict maternal effects in the sociable weaver, Philetairus socius, a species that lives in massive communal nests which may be occupied by only a few to 100+ individuals in a single nest. This range of social environments is associated with variation in a number of phenotypic and life-history traits. We investigate whether maternal effects are adjusted accordingly. We found no evidence for the prediction that females might benefit from modifying brood hierarchies through an increased deposition of androgens with laying order. Instead, females appear to exacerbate brood reduction by decreasing the costly production of yolk mass and antioxidants with laying order. Additionally, we found that this effect did not depend on colony size. Finally, in accordance with an expected increased intensity of environmental stress with increasing colony size, we found that yolk androgen concentration increased with colony size. This result suggests that females may enhance the competitive ability of offspring raised in larger colonies, possibly preparing the offspring for a competitive social environment.

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

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

Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler.

In male birds, testosterone (T) plays an important role in aggressive and mate-attraction behaviour. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, extra-group copulations (EGCs) occur frequently, but are not accompanied by sexual courtship displays as in within-pair copulations. Paternity is nearly always gained by primary males. We investigated whether T levels and sperm storage capability (cloacal protuberance (CP)) in adult primary and subordinate males were related to timing of egg laying, levels of cuckoldry and extra-group paternity (EGP) opportunities. During the sexually active period before egg laying, T levels and CP were only elevated or enlarged (respectively) in primary males, and some suggestion was found that subordinate males do not invest in elevated T levels. The peak in T occurred during the fertile period of the female partner and corresponded to the peak period of male sexual displays and mate guarding, but was independent of cuckoldry risk (density of neighbouring primary males). CP was also enhanced during this period; however, CP but not T remained elevated after egg laying by their mates, and CP but not T was positively related to EGP opportunities (density of neighbouring fertile females). We conclude that T is involved in sexual courtship displays and mate guarding, but not in gaining EGCs. These findings contrast with those in other species where EGP involves elaborate sexual displays.

Consistent variation in yolk androgens in the Australian Brush-turkey, a species without sibling competition or parental care.

Maternal hormones are an excellent pathway for the mother to influence offspring development, and birds provide exceptional opportunities to study these hormone-mediated maternal effects. Two dominant hypotheses about the function of yolk androgens in avian eggs concern maternal manipulation of sibling competition and post hatching paternal care. In megapodes, however, neither sibling competition nor post hatching parental care exists. Eggs are incubated by external heat sources, and chicks dig themselves out of their underground nest and live independently of their parents and their siblings. In this first study on egg androgens of such a megapode, the Australian Brush-turkey Alectura lathami, we found nevertheless substantial amounts of maternal androgens. Since size of the incubation mound, incubation temperature, egg size and laying date greatly vary in this species, we analysed variation in testosterone (T), androstenedione (A4) and dihydrotestosterone (DHT) in relation to these factors. T concentrations were significantly higher in eggs from bigger mounds and laid at greater depth, which may compensate via anabolic effects for the longer duration and higher energetic requirements of chicks when digging themselves out. T concentrations were higher in smaller eggs, and both yolk A4 and T concentrations increased with laying date, perhaps as a compensatory measure, while DHT concentrations only varied across different mounds. These results indicate that maternal androgens may influence offspring development outside the contexts of sibling competition or parental care.

Avian mothers create different phenotypes by hormone deposition in their eggs.

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

Balancing between costs and benefits of maternal hormone deposition in avian eggs.

Avian eggs contain substantial amounts of maternal androgens, and several studies have indicated that these are beneficial for the chick. Nevertheless, there is a large and systematic variation in maternal hormone concentrations both within and between clutches. If maternal androgens also involve costs, this might explain why not all mothers put high levels of androgens in their clutches. However, the simultaneous occurrence of both benefits and costs has not yet been convincingly demonstrated. We show experimentally that yolk androgens suppress immune function and simultaneously stimulate growth in black-headed gull chicks. Thus, mothers face a trade-off between these costs and benefits and may tune hormone deposition to prevailing conditions that influence chick survival.

Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth.

Hormones of maternal origin are known to be transferred to the egg yolks of oviparous species. Several studies have shown that within and between clutch variation of maternal androgens may be adaptively tuned. Moreover, it has recently been hypothesized that sex steroids of maternal origin may play a role in adaptive sex ratio manipulation. For sex determination the eggs have to be incubated to allow the germinal disc to grow and thus extract sufficient DNA. This means that yolk hormone levels are determined after a number of days of incubation and this may hamper interpretation of the data. If yolk utilization or embryonic hormone production are influenced by the sex of the embryo, differences in hormone content at a certain stage of incubation do not reflect the mother's initial allocation. In this experiment we show that testosterone levels in chicken eggs do not change with incubation period. A4 levels decrease between 3 and 5 days of incubation, which we cannot explain. Male eggs did not contain higher levels of testosterone or androstenedione than female eggs, in contrast to the data reported for another galliform species, the peacock. We conclude that it is unlikely that maternal androgens are a key factor in the avian sex determination mechanism.

Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull.

Within- and between-clutch variation in yolk titres of hormones of maternal origin has been found in many avian species. So far, experiments have revealed mainly beneficial effects of maternal androgens. This would also apply to black-headed gulls (Larus ridibundus). Previous experiments have shown that chicks benefit from these higher levels since their competitive abilities are improved and growth and survival probabilities thus enhanced. However, not all females show the same increase in yolk hormones from first to last egg or invest equally high amounts of androgens in their clutches. Possibly, there is a trade-off between the beneficial effects of high androgen levels and potential costs, such as increased metabolic rates. We studied possible metabolic costs of experimentally elevated yolk androgen levels for chicks of several age classes, starting three days prior to hatching until fledging at an age of approximately 30 days. Daily energy expenditure in the field, measured using the doubly labelled water technique, did not differ between treatments or between sexes. Oxygen consumption measured in birds at rest in the lab (RMR) did not vary between chicks hatched from androgen-injected (T) or oil-injected (Oil) control eggs at any age in thermo-neutral or below thermo-neutral conditions. Males showed a lower RMR than females towards the fledging age. We conclude that it is unlikely that the costs of high maternal androgen levels can be found in higher energy expenditure in the chick.