Claudio Carere

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.

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.

Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress.

A standard handling protocol was used to test the hypothesis that boldness predicts stress responsiveness in body temperature and breath rate. Great tit (Parus major) nestlings were taken from the field, hand reared until independence, and their response to a novel object was assessed. At the age of 6 months, during the active phase (daytime), body temperature was recorded and breath rate was counted immediately after capture and after 5 min of quiet rest in a bag. A second group of birds of two lines bidirectionally selected for the same trait was tested during the inactive phase (nighttime). During the active phase, body temperature and breath rate were higher in the first than in the second measurement. In the second measurement, shy individuals showed higher body temperature than bold individuals. In the inactive phase, values of both parameters were lower than in the active phase. Body temperature was lower in the first measurement than in the second measurement and no line difference emerged. Breath rate was higher in shy than in bold individuals and did not differ between the two measurements. Females had higher body temperatures than males, probably due to their lower weight, because body temperature was negatively correlated with body mass. The results indicate that body temperature and breath rate are indicators of acute stress in songbirds and that differences in personality traits during the juvenile phase are reflected in differential stress responsiveness later in life.

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.

Sexual versus individual differentiation: the controversial role of avian maternal hormones.

Avian embryos are exposed not only to endogenous sex steroids, which are produced by their gonads and have a key role in sexual differentiation, but also to maternal steroids transferred into the egg yolk, which can modulate the development of individual differences in behavior. Studies of maternal hormones have primarily focused on ultimate questions (evolutionary trade-offs, functional significance), whereas proximate mechanistic questions have been largely ignored. A central problem that must be addressed is how exposure to maternal hormones affects the individual phenotype without interfering with sexual differentiation. Separate effects could result from the action of different hormones, at different doses or at different times, on different targets.

Effect of social defeat in a territorial bird (Parus major) selected for different coping styles

We addressed the questions (i) whether a social defeat triggers similar autonomic and behavioral responses in birds as is known from mammals and (ii) whether individuals that differ in coping style differ in their reaction to a social defeat. Adult captive male great tits (Parus major) from either of two different selection lines for coping style were used to test the effect of social defeat by an aggressive resident male conspecific on subsequent social and nonsocial behaviour, body temperature, breath rate and body mass. These parameters were measured 1 day before (baseline), immediately after and at Days 1 to 3 and 6 after the social interaction took place (Day 0). Social defeat decreased social exploration and increased body temperature substantially for at least 1 day in all birds. Breath rate and body mass were not affected. Birds belonging to the more aggressive and bolder line showed impairment in activity immediately after the social defeat. This is to our knowledge the first report showing that psychosocial stress in birds can have a similar impact as in rodents, but with a shorter recovery time. This might be due to species-specific differences in sensitivity to social stress, or to differences in the way social stress was induced.

Stopover decision during migration: Physiological conditions predict nocturnal restlessness in wild passerines

During migration, a number of bird species rely on stopover sites for resting and feeding before and after crossing ecological barriers such as deserts or seas. The duration of a stopover depends on the combined effects of environmental factors, endogenous programmes and physiological conditions. Previous studies indicated that lean birds prolong their refuelling stopover compared with fat birds; however, the quantitative relationship between physiological conditions and stopover behaviour has not been studied yet. Here, we tested in a large sample of free-living birds of three European passerines (whinchats, Saxicola rubetra, garden warblers, Sylvia borin and whitethroats, Sylvia communis) whether the amount of migratory restlessness (Zugunruhe) shown at a stopover site depends on physiological conditions. An integrated measure of condition based on body mass, amount of subcutaneous fat and thickness of pectoral muscles strongly predicted the intensity of Zugunruhe shown in recording cages in the night following capture. These results provide novel and robust quantitative evidence in support of the hypothesis that the amount of energy reserves plays a major role in determining the stopover duration in migratory birds.

Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool

Large-scale studies are essential to assess the emission patterns and spatial distribution of organohalogenated pollutants (OHPs) in the environment. Bird eggs have several advantages compared to other environmental media which have previously been used to map the distribution of OHPs. In this study, large-scale geographical variation in the occurrence of OHPs, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs), was investigated throughout Europe using eggs of a terrestrial residential passerine species, the great tit (Parus major). Great tit eggs from 22 sampling sites, involving urban, rural and remote areas, in 14 European countries were collected and analysed (5-8 eggs per sampling site). The environmentally most important congeners/compounds of the analysed pollutants were detectable in all sampling locations. For PCBs, PBDEs and OCPs, no clear geographical contamination pattern was found. Sum PCB levels ranged from 143 ng/g lipid weight (lw) to 3660 ng/g lw. As expected, PCB concentrations were significantly higher in the sampled urban compared to the remote locations. However, the urban locations did not show significantly higher concentrations compared to the rural locations. Sum PBDEs ranged from 4.0 ng/g lw to 136 ng/g lw. PBDEs were significantly higher in the urbanized sampling locations compared to the other locations. The significant, positive correlation between PCB and PBDE concentrations suggests similar spatial exposure and/or mechanisms of accumulation. Significantly higher levels of OCPs (sum OCPs ranging from 191 ng/g lw to 7830 ng/g lw) were detected in rural sampling locations. Contamination profiles of PCBs, PBDEs and OCPs differed also among the sampling locations, which may be due to local usage and contamination sources. The higher variance among sampling locations for the PCBs and OCPs, suggests that local contamination sources are more important for the PCBs and OCPs compared to the PBDEs. To our knowledge, this is the first study in which bird eggs were used as a monitoring tool for OHPs on such a large geographical scale.