Social Influences during Adolescence on Adult Behaviour in Zebra Finches (Taeniopygia guttata) - Underlying Mechanisms and Functional Consequences

Bölting S. Social Influences during Adolescence on Adult Behaviour in Zebra Finches (Taeniopygia guttata) - Underlying Mechanisms and Functional Consequences. Bielefeld: Universität Bielefeld; 2018.An individual`s adult phenotype is not only influenced by its genetic predisposition, but also by environmental factors during ontogeny. This developmental plasticity enables an organism to produce a phenotype that is adapted to current or predicted future environmental conditions, enhancing the fitness of the individual at some point during its life. In many species, social influences during the prenatal and early postnatal period have long-lasting consequences for adult social behaviour. Lately, the adolescent life stage is being considered as another important developmental period of enhanced plasticity in which adult behaviour can be shaped. However, not much is known yet about the underlying mechanisms and fitness consequences of long-lasting behavioural modifications induced during adolescence. Based on research in mammals, it has been suggested that differences in social interactions modulate the secretion of sex steroid and glucocorticoid hormones, which in turn affect physiological maturation and the display of adult behaviour with consequences for fitness. In general, a more complex social environment has been proposed to improve adult social performance via increased social interactions. The aim of this thesis was to investigate the mechanisms and consequences of variation in adult behavioural phenotypes induced by differences in the social environment during adolescence in a social avian species, the zebra finch (Taeniopygia guttata). Zebra finches are monogamous songbirds usually living and breeding in large colonies, but especially during the breeding season, the size of colonies can differ considerably. In addition, some pairs breed more solitarily at a distance from other pairs rather than in the colony. This might crucially affect social interactions of individuals during development, which in turn might influence maturational parameters and adult behavioural performance. An earlier study in which male zebra finches were kept in pairs or groups of juveniles during adolescence in the lab has shown that those males differ in the frequency of adult courtship and aggressive behaviour, which may represent adaptive behavioural modifications. In the first study of this thesis, summarised in chapter 2, I investigated whether males reared in pairs or in groups of only juveniles, or in groups of juveniles and adults differ in the frequency of social interactions, endocrinological profiles (testosterone, corticosterone) and the development of adult song and adult plumage colouration during adolescence. Furthermore, I examined whether differences in developmental traits came along with differences in adult courtship and aggressive behaviour. I found that group-reared males had more social interactions and matured faster during adolescence than pair-reared males. In addition, group-reared males showed more courtship and aggression in adulthood, even though the strength of these effects differed between groups with and without adults. This suggests that effects of the adolescent social environment on adult behaviour in zebra finches are mediated via changes in social interactions and their effects on physiological processes underlying maturation. However, there was no evidence that the long-lasting differences in behaviour were related to changes in testosterone or corticosterone levels. Finally, the results further indicated that group-reared males differed from pair-reared males in their ability to adjust their behaviour to different types of interaction partners. They showed a high level of aggression towards socially less experienced and hence potentially inferior pair-reared opponents, but a low level of aggression towards equally skilled group-reared rivals. Pair-reared males did not show any adjustment of aggression to their opponents’ characteristics. This might indicate a higher social competence of group-reared males, and is likely to affect fitness, for example by facilitating access to females when competing against inferior rivals. In chapter 3, I further investigated the ability of males to adjust the expression of courtship and aggression as a function of available social information. Males were singly introduced into an unfamiliar flock of established breeding pairs and additional unpaired females. The mating status of conspecifics is especially important in a monogamous group-living species, such as the zebra finch, because the chance to secure a mate and the risk to get involved in costly fights depend on appropriate courtship and aggression shown towards potential mates and competitors. All males showed more courtship song towards unpaired females than towards paired females, and males from different rearing conditions did not differ in how much they preferred singing towards unpaired females. As found previously, pair-reared males showed overall less courtship singing than group reared males. These results suggest that there is no difference in the ability to assess the suitability of females as potential mates between male zebra finches from the different social rearing environments. However, males appear to differ in how they compete with opponents. All males directed more aggression towards males than towards females, but group-reared males discriminated significantly more between male and female interaction partners than pair-reared males. These effects may be adaptive, because increased courtship singing and fighting skills of group-reared males might increase their attractiveness and competitiveness, and thereby influence their fitness in complex social settings. In the study summarised in chapter 4, I focused on the consequences of variation in courtship and aggression of males from different social rearing environments during adolescence for reproductive success. A complex social context with high potential for females to be selective during mate choice and with high male competition was chosen, because differences in courtship and aggression, which potentially affect attractiveness and competitiveness, are most likely to have the strongest effect under such conditions. Males reared in juvenile pairs, juvenile groups and mixed-age groups during adolescence were introduced into an aviary with a limited number of females and were allowed to breed. I found that more group-reared males obtained paternity than pair-reared males. In addition, group reared males sired a larger number of offspring in a larger number of nests and often attained multiple paternities. The increased reproductive success of group-reared males compared to pair reared males indicates that zebra finch males reared in an enriched social environment during adolescence are adapted to a life under complex social conditions in adulthood. An increased attractiveness and competitiveness may enable group-reared individuals to accrue fitness gains in such an environment through higher mating success and increased extra-pair paternities. In conclusion, my findings support the idea of adolescence as a sensitive period in which adult behaviour can be shaped by the social environment in zebra finches. Moreover, I present, for the first time, evidence that the effects of the adolescent social environment on adult behaviour may be mediated via changes in social interactions, affecting physiological maturation of individuals. A higher frequency of interactions in an enriched social environment seems to accelerate maturation of zebra finch males and to result in behavioural modifications that are beneficial under complex social conditions with high competition in later life. Hence, this thesis provides the first evidence for adaptive phenotypic shaping by the social environment during adolescence in zebra finches

Effects of the social environment during adolescence on the development of social behaviour, hormones and morphology in male zebra finches (Taeniopygia guttata)

Abstract Background Individual differences in behaviour are widespread in the animal kingdom and often influenced by the size or composition of the social group during early development. In many vertebrates the effects of social interactions early in life on adult behaviour are mediated by changes in maturation and physiology. Specifically, increases in androgens and glucocorticoids in response to social stimulation seem to play a prominent role in shaping behaviour during development. In addition to the prenatal and early postnatal phase, adolescence has more recently been identified as an important period during which adult behaviour and physiology are shaped by the social environment, which so far has been studied mostly in mammals. We raised zebra finches ( Taeniopygia guttata ) under three environmental conditions differing in social complexity during adolescence\ua0-\ua0juvenile pairs, juvenile groups, and mixed-age groups - and studied males\u2019 behavioural, endocrine, and morphological maturation, and later their adult behaviour. Results As expected, group-housed males exhibited higher frequencies of social interactions. Group housing also enhanced song during adolescence, plumage development, and the frequency and intensity of adult courtship and aggression. Some traits, however, were affected more in juvenile groups and others in mixed-age groups. Furthermore, a testosterone peak during late adolescence was suppressed in groups with adults. In contrast, corticosterone concentrations did not differ between rearing environments. Unexpectedly, adult courtship in a test situation was lowest in pair-reared males and aggression depended upon the treatment of the opponent with highest rates shown by group-reared males towards pair-reared males. This contrasts with previous findings, possibly due to differences in photoperiod and the acoustic environment. Conclusion Our results support the idea that effects of the adolescent social environment on adult behaviour in vertebrates are mediated by changes in social interactions affecting behavioural and morphological maturation. We found no evidence that long-lasting differences in behaviour reflect testosterone or corticosterone levels during adolescence, although differences between juvenile and mixed-age groups suggest that testosterone and song behaviour during late adolescence may be associated