Hubert Schwabl

Maternal testosterone in the avian egg enhances postnatal growth.

The eggs of the canary (Serinus canaria) contain variable doses of maternal testosterone. The reported experiments investigated whether testosterone influences nestling growth and how this interacts with differences of the growth of nest mates that are caused by asynchronous hatching. Injections of testosterone into the yolk of unincubated eggs enhanced the growth after hatching compared to nestlings that had hatched simultaneously from control eggs. These differences were established within 22 hr of hatching. Exogenous testosterone promoted growth in both sexes and there was no sexual difference in the growth of control birds. Testoster-one-treated chicks also begged more often for food. Previous studies have shown that the content of maternal testosterone increases in each subsequently laid egg in a clutch. Consistent with the results obtained by testosterone injections nestlings that hatched from eggs with higher concentrations of maternal testosterone grew faster compared to chicks that hatched synchronously from eggs with lower testosterone concentrations. However, more testosterone did not compensate for reduced growth that was caused by later hatching due to asynchronous incubation of clutches. This direct effect of maternal testosterone on growth in combination with a flexible onset of incubation allows to selectively enhance the growth and fitness of individual offspring of a brood.

Maternal androgens in black-headed gull ( Larus ridibundus ) eggs: consequences for chick development

We tested the hypothesis that mother birds counterbalance the negative effects of hatching asynchrony for later–hatched chicks by increasing the yolk androgen concentrations in consecutive eggs of their clutch. In doing so, they may adaptively tune each offsprings competitive ability and, thus, growth and survival. However, evidence in support of this hypothesis is contradictory. The yolk concentrations of maternal androgens in the eggs of black–headed gulls increase significantly with the laying order of the eggs in a clutch. We experimentally tested the functional consequences of this increase on chick development under natural conditions by injecting eggs with either an oil or androgen solution. We created experimental clutches in which androgen levels either stayed constant or increased with laying order while controlling for differences in egg quality by using only first–laid eggs. We then compared development, growth and survival between these broods. Androgen treatment enhanced embryonic development because androgen–treated eggs hatched half a day earlier than controls, while their size at hatching was similar to oil–treated controls. Androgen treatment did not increase chick survival, but it enhanced growth. Androgen–treated, third–hatched chicks had a higher body mass and longer legs than thirdndash;hatched chicks that hatched from oil–treated eggs. At the same time, growth of first chicks (which were all oil treated) was reduced by the presence of two androgen–treated siblings, suggesting that yolk androgens enhance the competitive ability of later–hatched chicks. Our results support the hypothesis that transfer of different amounts of androgens to the eggs of a clutch is a mechanism by which mothers maximize their reproductive output.

Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?

Over the past decade, birds have proven to be excellent models to study hormone-mediated maternal effects in an evolutionary framework. Almost all these studies focus on the function of maternal steroid hormones for offspring development, but lack of knowledge about the underlying mechanisms hampers further progress. We discuss several hypotheses concerning these mechanisms, point out their relevance for ecological and evolutionary interpretations, and review the relevant data. We first examine whether maternal hormones can accumulate in the egg independently of changes in hormone concentrations in the maternal circulation. This is important for Darwinian selection and female physiological trade-offs, and possible mechanisms for hormone accumulation in the egg, which may differ among hormones, are reviewed. Although independent regulation of plasma and yolk concentrations of hormones is conceivable, the data are as yet inconclusive for ovarian hormones. Next, we discuss embryonic utilization of maternal steroids, since enzyme and receptor systems in the embryo may have coevolved with maternal effect mechanisms in the mother. We consider dose–response relationships and action pathways of androgens and argue that these considerations may help to explain the apparent lack of interference of maternal steroids with sexual differentiation. Finally, we discuss mechanisms underlying the pleiotropic actions of maternal steroids, since linked effects may influence the coevolution of parent and offspring traits, owing to their role in the mediation of physiological trade-offs. Possible mechanisms here are interactions with other hormonal systems in the embryo. We urge endocrinologists to embark on suggested mechanistic studies and behavioural ecologists to adjust their interpretations to accommodate the current knowledge of mechanisms.

Yolk androgens reduce offspring survival

Females may favour some offspring over others by differential deposition of yolk hormones. In American kestrels (Falco sparverius), we found that yolks of eggs laid late in the sequence of a clutch had more testosterone (T) and androstenedione (A4) than yolks of first–laid eggs. To investigate the effects of these yolk androgens on nestling ‘fitness’, we injected both T and A4 into the yolks of first–laid eggs and compared their hatching time, nestling growth and nestling survival with those of first–laid eggs in which we injected vehicle as a control. Compared to controls, injection of T and A4 at a dose intended to increase their levels to those of later–laid eggs delayed hatching and reduced nestling growth and survival rates. Yolk androgen treatment of egg 1 had no effect on survival of siblings hatching from subsequently laid eggs. The adverse actions of yolk androgen treatment in the kestrel are in contrast to the favourable actions of yolk T treatment found previously in canaries (Serinus canaria). Additional studies are necessary in order to determine whether the deposition of yolk androgens is an adaptive form of parental favouritism or an adverse by–product of endocrine processes during egg formation. Despite its adaptive significance, such ‘transgenerational’ effects of steroid hormones may have helped to evolutionarily shape the hormonal mechanisms regulating reproduction.

Maternal investment. Sex differences in avian yolk hormone levels.

It has been suggested that female birds put more resources into eggs fathered by attractive males by laying larger eggs or by adding more testosterone, but this inference could be undermined if eggs of different sex are provisioned differently, as these studies did not control for sex differences. Here we compare hormone concentrations in the yolks of male and female eggs and find that these are significantly different. Our results indicate that it is premature to conclude that female birds invest more in eggs sired by a preferred male, and raise the possibility that yolk sex steroids may be part of the sex-determining process in birds.

Maternal testosterone in tree swallow eggs varies with female aggression

Variation in the investment of maternal resources in eggs, such as proteins and lipids, can have a profound influence on the growth and development of young. Maternal resources transferred to eggs also include androgens found in the yolk. In several species of birds the concentration of testosterone in the yolk either increases or decreases with laying order. Yolk testosterone has been shown to have various effects on the young including enhanced growth and dominance as well as reduced survival. Previous work suggested that the concentration of testosterone in the yolk may be influenced by the females social conditions, specifically the frequency of aggressive interactions. In tree swallows, Tachycineta bicolor, we found that yolk testosterone was correlated with the aggressive interactions of the female before and during egg laying. In contrast to other species, yolk testosterone did not vary with laying order in tree swallows. Thus, patterns of yolk testosterone are more variable than thought previously and may be influenced by the social conditions experienced by the female during laying.

Endocrine Mechanisms of Migration

Migration involves complex interrelationships of anabolic and catabolic metabolism, behavior, and reproductive development. Vernal migration (the movement of individuals from the wintering area to the breeding area) occurs during a period of gonadal development and increasing levels of reproductive hormones. Autumnal migration (the movement of individuals from the breeding area to wintering grounds) occurs after the breeding season when the gonads have regressed to a completely inactive state, and circulating levels of reproductive hormones are basal (e.g., Farner 1955; Wingfield and Farner 1980). Note that juveniles also undergo autumnal migration. Since the two migratory periods occur in radically different physiologic states, it is reasonable to suspect that the factors timing and controlling at least the preparations for migration will be different. On the other hand, both migratory states have common requirements, e.g., for hyperphagia, fat deposition (as fuel for long flights), and migratory flight itself. Thus, it is likely that some of the regulatory mechanisms of migration will be similar in spring and autumn and others different.

Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition

How much effort to expend in any one bout of reproduction is among the most important decisions made by an individual that breeds more than once. According to life-history theory, reproduction is costly, and individuals that invest too much in a given reproductive bout pay with reduced reproductive output in the future. Likewise, investing too little does not maximize reproductive potential. Because reproductive effort relative to output can vary with predictable and unpredictable challenges and opportunities, no single level of reproductive effort maximizes fitness. This leads to the prediction that individuals possessing behavioural mechanisms to buffer challenges and take advantage of opportunities would incur fitness benefits. Here, we review evidence in birds, primarily of altricial species, for the presence of at least two such mechanisms and evidence for and against the seasonal coordination of these mechanisms through seasonal changes in plasma concentrations of the pituitary hormone prolactin. First, the seasonal decline in clutch size of most bird species may partially offset a predictable seasonal decline in the reproductive value of offspring. Second, establishing a developmental sibling-hierarchy among offspring may hedge against unpredictable changes in resource availability and offspring viability or quality, and minimize energy expenditure in raising a brood. The hierarchy may be a product, in part, of the timing of incubation onset relative to clutch completion and the rate of yolk androgen deposition during the laying cycle. Because clutch size should influence the effects of both these traits on the developmental hierarchy, we predicted and describe evidence in some species that females adjust the timing of incubation onset and rate of yolk androgen deposition to match clutch size. Studies on domesticated precocial species reveal an inhibitory effect of the pituitary hormone prolactin on egg laying, suggesting a possible hormonal basis for the regulation of clutch size. Studies on the American kestrel (Falco sparverius) and other species suggest that the seasonal increase in plasma concentrations of prolactin may regulate both a seasonal advance in the timing of incubation onset and a seasonal increase in the rate of yolk androgen deposition. These observations, together with strong conceptual arguments published previously, raise the possibility that a single hormone, prolactin, functions as the basis of a common mechanism for the seasonal adjustment of reproductive effort. However, a role for prolactin in regulating clutch size in any species is not firmly established, and evidence from some species indicates that clutch size may not be coupled to the timing of incubation onset and rate of yolk androgen deposition. A dissociation between the regulation of clutch size and the regulation of incubation onset and yolk androgen deposition may enable an independent response to the predictable and unpredictable challenges and opportunities faced during reproduction.

Ectoparasite-modulated deposition of maternal androgens in great tit eggs.

Maternal yolk androgens can promote growth and competitive abilities of nestling birds but are also suggested to increase susceptibility to parasites or suppress immune function. We tested the hypothesis that females exposed to ectoparasites during egg formation will adjust the content of androgens in the yolk. We predicted that when anticipating high levels of parasitism, females deposit (i) less androgens into all eggs of their clutch and (ii) smaller amounts of androgens in eggs late in the laying sequence to facilitate brood reduction.In a field experiment we exposed female great tits (Parus major) to hen fleas (Ceratophyllus gallinae), or kept them free of ectoparasites prior to egg laying. We collected the eggs and measured yolk concentrations of androstenedione (A4), testosterone (T) and 5∝–dihydrotestosterone (DHT) by radioimmunoassay. Among clutches, eggs of ectoparasite–exposed females contained significantly less A4 and tended to contain less T, whereas DHT content was unaffected. Within clutches, content of A4 and T increased significantly with laying order whereas DHT content significantly decreased. These patterns were unaffected by ectoparasites. In summary, our results provide no evidence for hormone–based facilitation of brood reduction under ectoparasite exposure but support the hypothesis that females exposed to ectoparasites reduce levels of T and its precursor A4 in yolk and might thereby reduce the negative effects of parasites on offspring.

The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions.

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