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

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          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 - juvenile pairs, juvenile groups, and mixed-age groups - and studied males’ 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.

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          Most cited references79

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          The adolescent brain and age-related behavioral manifestations.

          L Spear (2000)
          To successfully negotiate the developmental transition between youth and adulthood, adolescents must maneuver this often stressful period while acquiring skills necessary for independence. Certain behavioral features, including age-related increases in social behavior and risk-taking/novelty-seeking, are common among adolescents of diverse mammalian species and may aid in this process. Reduced positive incentive values from stimuli may lead adolescents to pursue new appetitive reinforcers through drug use and other risk-taking behaviors, with their relative insensitivity to drugs supporting comparatively greater per occasion use. Pubertal increases in gonadal hormones are a hallmark of adolescence, although there is little evidence for a simple association of these hormones with behavioral change during adolescence. Prominent developmental transformations are seen in prefrontal cortex and limbic brain regions of adolescents across a variety of species, alterations that include an apparent shift in the balance between mesocortical and mesolimbic dopamine systems. Developmental changes in these stressor-sensitive regions, which are critical for attributing incentive salience to drugs and other stimuli, likely contribute to the unique characteristics of adolescence.
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            Collecting baseline corticosterone samples in the field: is under 3 min good enough?

            Evaluating corticosterone (CORT) responses to stress in free-living vertebrates requires knowing the unstressed titers prior to capture. Based upon laboratory data, the assumption has been that samples collected in less than 3 min of capture will reflect these unstressed concentrations. This assumption was tested for six species using samples collected from 945 individuals at 0-6 min after capture. Samples were from five avian species trapped at multiple times of year and one reptilian species, comprising a total of 14 different data sets for comparisons. For seven of 14 data sets, including five species, there was no significant increase in corticosterone titers within 3 min of capture. In six of the 14 data sets, corticosterone titers increased significantly after 2 min, and in one data set, the increase started at 1.5 min. In all seven of the cases showing an increase before 3 min, however, corticosterone titers from the time of increase to 3 min were significantly lower than titers after 30 min of restraint stress. These results indicate a high degree of confidence for these species that samples collected in less than 2 min reflect unstressed (baseline) concentrations, and that samples collected from 2-3 min also will likely reflect baseline concentrations but at worst are near baseline.
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              Social Learning in Animals: Empirical Studies and Theoretical Models

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                Author and article information

                Contributors
                stefanie.boelting@uni-bielefeld.de
                nvengelhardt@gmx.de
                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                25 January 2017
                25 January 2017
                2017
                : 14
                : 5
                Affiliations
                [1 ]ISNI 0000 0001 0944 9128, GRID grid.7491.b, Department of Animal Behaviour, , Bielefeld University, ; 33615 Bielefeld, Germany
                [2 ]ISNI 0000 0001 2219 0747, GRID grid.11201.33, Faculty of Science and Engineering, , University of Plymouth, ; Drake Circus, Plymouth, PL4 8AA UK
                Author information
                http://orcid.org/0000-0001-5209-4967
                Article
                190
                10.1186/s12983-017-0190-4
                5267386
                6dd53505-bbec-42b8-ad53-c5d59cb2ff4d
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 14 November 2016
                : 18 January 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, German Research Foundation (DFG);
                Award ID: DFG, FOR 1232: EN922/2-2
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Animal science & Zoology
                social environment,adolescence,social interactions,maturation,testosterone,corticosterone,plumage colouration,courtship,aggression,song

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