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

Abstract

BackgroundIndividual 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 - juvenile pairs, juvenile groups, and mixed-age groups - and studied males’ behavioural, endocrine, and morphological maturation, and later their adult behaviour.ResultsAs 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.ConclusionOur 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.

Why and how the early-life environment affects development of coping behaviours

“…The influence of the presence and absence of a social group has also been studied in other species. Group housing in zebra finches ( T. guttata ), for example, was related to a higher number of social interactions in males (Bölting and von Engelhardt 2017 ). In cichlids ( N. pulcher ), fry raised with adults showed more aggressive and submissive behaviour to each other than fish raised with siblings only (Arnold and Taborsky 2010 ).…”

“…Lighter females showed no such difference (Guenther and Trillmich 2013 ). Related to this, it has been suggested that differences in photoperiod and acoustic environment were the cause for conflicting results between studies into zebra finches’ ( T. guttata ) social behaviour (Bölting and von Engelhardt 2017 ). In dogs, the largest environmental factor associated with separation anxiety and stress sensitivity to noise was the amount of daily exercise during early life (Tiira and Lohi 2015 ).There is a growing interest in human-influenced effects on behavioural development, often in the context of global change, on topics including human disturbance, ecological stressors, temperature and climate variability, several of which are reviewed in Love et al ( 2013 ).…”

Multiple behavioural mechanisms shape development in a highly social cichlid fish

“…Early-life social environments and experiences are potent drivers of developmental plasticity for social species and, as a result, can have strong, long-term effects on organismal phenotype (Bateson, 2001;Bateson et al, 2004;Kuijper & Johnstone, 2019;Taborsky, 2017;Weaver, 2009). Early-life social effects have been documented across vertebrate taxa (e.g., (Arnold & Taborsky, 2010;Bölting & von Engelhardt, 2017;Champagne & Curley, 2005;Moretz et al, 2007;Perkeybile & Bales, 2017;White et al, 2010), yet the specific attributes of early social environments and experiences that cause phenotypic changes are often unidentified (Kasumovic, 2013;Taborsky, 2016). Social interactions and stimuli can make up a substantial part of juvenile experience.…”

“…Social interactions and stimuli can make up a substantial part of juvenile experience. Depending on the species and group structure, early social interactions can involve parents (maternal, paternal, or biparental care) (Champagne & Curley, 2005;McClelland et al, 2011;Perkeybile et al, 2013), parental helpers (Arnold & Taborsky, 2010;Taborsky et al, 2012), siblings (Branchi et al, 2013;Buist et al, 2013;D'Andrea et al, 2007;Monclús et al, 2012), peers (Ahloy Dallaire & Mason, 2017;Bölting & von Engelhardt, 2017;Förster & Cords, 2005;Moretz et al, 2007;Weinstein et al, 2014), and other members of the group (Bray, Murray, et al, 2021;Förster & Cords, 2005;Jin et al, 2015), as well as observations of others interacting (Clay & de Waal, 2013;Desjardins et al, 2012;Oliveira et al, 1998). Identifying the specific, proximate causes-the behavioral mechanisms-is critical to understanding how gene-by-environment interactions shape processes of developmental plasticity and behavioral developmental trajectories.…”

How Developmental and Behavioural Plasticity in the Field Cricket is Influenced by the Acoustic Social Environment and Anthropogenic Noise

“…In addition to development influencing adult body phenotype, aggressive behaviours can also be directly affected by the developmental social environment. For example, group reared male zebra finches (Taeniopygia guttata) are more aggressive than males reared in pair-groups (Bölting & Von Engelhardt 2017). Similarly, in veiled chameleons, (Chamaeleo calyptratusoups) males reared in groups are more aggressive than males reared in social isolation (Ballen et al 2014).…”