Ton G. G. Groothuis

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.

Avian personalities: characterization and epigenesis.

The work presented here aims at understanding the nature, epigenesis and function of personality types (here called behavioral profiles) in birds, focusing on a wild bird species, the great tit (Parus major). Lines bidirectionally selected for exploration show a wide array of social and non-social behavioral differences, and also some differences in physiological parameters. Line differences in these characteristics and their relationships show significant temporal consistency. The results show a surprising similarity between the great tit and a rodent model, suggesting a fundamental principle in the organization of behavioral profiles. The nature of this principle and whether or not it is multi-dimensional is discussed. However, the similarity with a chicken model is less clear, which points to some caution for generalization. The epigenesis of great tit behavioral profiles is discussed. Selection experiments with replication and backcrosses reveal a strong genetic basis, and suggest an influence of maternal effects. Ontogenetic manipulations indicate strong developmental plasticity, suggesting adaptive adjustment to prevailing environmental circumstances. They also show that behavioral characteristics belonging to the same profile can become uncoupled. Finally, field data on several fitness parameters of the different personalities in wild great tits are summarized. These data suggest that variation in selection pressure in time and space and assortative mating are plausible mechanisms accounting for the maintenance of different behavioral profiles within the same population.

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.

Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress

In this study we tested the hypothesis that in a passerine bird (great tit, Parus major) individuals differing for coping strategies differ in the magnitude of the adrenocortical response to social stress as well. Furthermore, we aimed at characterizing daily rhythms in corticosteroid release before and after social stress. We used 16 males from either of two lines bidirectionally selected for different coping strategies (fast and slow explorers). Social stress was induced by confrontation with an aggressive resident male. Corticosteroid metabolites were analyzed in feces collected at 90-min intervals from 900 to 1630 h on a baseline day, on the day of the social conflict, and on the following day. In both days and in both lines levels varied with time of day in a robust rhythm with a peak in the first sample of the morning and a trough at the end of the light phase. This rhythm correlates with activity (perch hopping). An overall increase in levels relative to baseline day was observed between 30 and 140 min after the challenge. Birds of the less aggressive and more cautious line (slow explorers) showed a trend for a higher response compared to birds of the more aggressive and bolder line (fast explorers), which showed almost no response. On the day after the challenge the birds of the slow line exhibited significantly reduced corticosteroid secretion, probably due to an increased negative feedback. The results provide evidence for a physiological basis of different coping strategies in birds, emerging in response to social stress and with a pattern similar to that in other vertebrates.

Personalities in great tits, Parus major : stability and consistency

We carried out a longitudinal study on great tits from two lines bidirectionally selected for fast or slow exploratory performance during the juvenile phase, a trait thought to reflect different personalities. We analysed temporal stability and consistency of responses within and between situations involving exploratory and sociosexual behaviour. Exploratory behaviour was assessed both in the juvenile phase and in adulthood (2–3-year interval) by means of a novel object test and an open field test. We assessed agonistic behaviour twice in adulthood with a 7-month interval by confronting males with either a caged or a free-moving intruder. We assessed sexual behaviour in adulthood by presenting two caged conspecifics of the opposite sex. Exploratory scores still differed between the lines at both ages; however, slow birds became faster with age and were less stable than fast birds. Slow explorers spent more time in agonistic displays and took longer to attack than fast birds. Slow birds also took longer than fast birds to approach a member of the opposite sex. We conclude that, at the level of line, behavioural differences were stable over time and extended to other situations. At the individual level, consistency across time and situations was less evident overall, but fast birds tended to be more consistent than slow birds. Slow explorers could be described as reactive copers, showing a relatively high degree of behavioural plasticity, and fast explorers as proactive, in line with similar studies in rodents.

Yolk androgens and begging behaviour in black-headed gull chicks : an experimental field study

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.

Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences

Developmental processes can have major impacts on the correlations in behaviour across contexts (contextual generality) and across time (temporal consistency) that are the hallmarks of animal personality. Personality can and does change: at any given age or life stage it is contingent upon a wide range of experiential factors that occurred earlier in life, from prior to conception through adulthood. We show how developmental reaction norms that describe the effects of prior experience on a given behaviour can be used to determine whether the effects of a given experience at a given age will affect contextual generality at a later age, and to illustrate how variation within individuals in developmental plasticity leads to variation in contextual generality across individuals as a function of experience. We also show why niche-picking and niche-construction, behavioural processes which allow individuals to affect their own developmental environment, can affect the contextual generality and the temporal consistency of personality. We conclude by discussing how an appreciation of developmental processes can alert behavioural ecologists studying animal personality to critical, untested assumptions that underlie their own research programmes, and outline situations in which a developmental perspective can improve studies of the functional significance and evolution of animal personality.

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.

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.