In mammals, the development of individual behavioral profiles can be influenced considerably by social factors during early phases of life. In guinea pigs, for instance, sons whose mothers experienced social instability during pregnancy and lactation show an infantilized behavioral profile. Here, we examined whether the same phenomenon exists also in wild cavies, the ancestor of the domestic guinea pig. Using a comparable experimental approach, our results revealed a similar behavioral infantilization as well as a delayed gonadal development of sons when their mothers had lived under unstable social conditions. These data show clearly that the behavioral and hormonal profile of male wild cavies can be shaped significantly by the social environment in which their mothers lived during pregnancy and lactation. Hence the underlying mechanisms cannot have been brought about by artificial selection during domestication. Rather, they represent maternal effects evolved through natural selection adjusting the offspring to the current environmental conditions.

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BackgroundThe social environment the mother experiences during pregnancy and lactation can powerfully influence the offspring’s behavioural profile. Our previous studies in wild cavies show that two different social environments during pregnancy and lactation bring about different behavioural strategies of male offspring later in life: An unstable social environment leads to a behavioural camouflage strategy, hypothesised to be beneficial at times of socially challenging situations. A stable social environment during early phases of life, however, leads to an early reproduction strategy, expected to be more successful at times of social stability. In the present study, we observed the behavioural strategies of the two types of males in direct comparison in a socially challenging situation: Two adolescent males were placed simultaneously in an unknown social group consisting of one adult male and two females in a semi-naturalistic environment. Cortisol as well as testosterone concentrations and activity levels were compared. Furthermore, paternities were analysed after the males reached sexual maturity. We hypothesised that sons showing a behavioural camouflage strategy are better adapted to cope with this socially challenging situation compared to those displaying an early reproduction strategy.ResultsAt the beginning of the experiment, no differences in plasma cortisol concentrations between the males were found, both showed a highly significant increase due to the challenging situation. From day 5 until the end of the experiment (duration = 40 days) sons showing an early reproduction strategy had significantly higher plasma cortisol concentrations compared with those showing a behavioural camouflage strategy. Plasma testosterone concentrations did not differ significantly. Activity levels decreased significantly over time independently of the male’s behavioural strategy. Both types of males did not sire offspring during the observation period.ConclusionHigher cortisol values from day 5 until the end of the experiment in sons showing an early reproduction strategy indicate higher levels of stress in these males compared to those displaying a camouflage strategy. We conclude that the modulation of the males behavioural strategy due to an unstable social environment during early development facilitates the endocrine adaptation to a comparable social situation later in life.

The prospective severity assessment in animal experiments in the categories' non-recovery, mild, moderate, and severe is part of each approval process and serves to estimate the harm/benefit. Harms are essential for evaluating ethical justifiability, and on the other hand, they may represent confounders and effect modifiers within an experiment. Catalogs and guidelines provide a way to assess the experimental severity prospectively but are limited in adaptation due to their nature of representing particular examples without clear explanations of the assessment strategies. To provide more flexibility for current and future practices, we developed the modular Where-What-How (WWHow) concept, which applies findings from pre-clinical studies using surgical-induced pain models in mice and rats to provide a prospective severity assessment. The WWHow concept integrates intra-operative characteristics for predicting the maximum expected severity of surgical procedures. The assessed severity categorization is mainly congruent with examples in established catalogs; however, because the WWHow concept is based on anatomical location, detailed analysis of the tissue trauma and other intra-operative characteristics, it enables refinement actions, provides the basis for a fact-based dialogue with authority officials and other stakeholders, and helps to identify confounder factors of study findings.

The social environment shapes the individual behavioural profile during early phases of life. In guinea pigs the behavioural profile of daughters whose mothers experienced social instability during pregnancy and lactation (UE-daughters) are behaviourally masculinised. Since guinea pigs are domesticated the question arises whether this phenomenon was brought about by domestication or whether it represents an adaptive behavioural mechanism inherited from their wild ancestor, the wild cavy. This study, therefore, investigates the effects of an early unstable social environment on the biobehavioural profile of daughters in wild cavies and compares these effects with the findings in the domestic form. Our results show higher frequencies of aggression and play behaviour in UE-daughters, indicating a comparable behavioural masculinisation as in guinea pigs. Thus, the observed behavioural changes in UE-daughters cannot have been brought about by artificial selection during domestication. Rather they represent maternal effects evolved through natural selection.