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Abstract: Understanding how birth origin (whether born in the wild or captivity) influences behavioural development is important for fundamental and applied ethology, especially when captive-bred (CB) individuals from wild species are used in research or conservation. CB animals are typically much more prone to stereotypic behaviour (SB) than are wild caught (WC) conspecifics, an effect which in striped mice is accompanied by increased tendencies to form behavioural routines. However, WC mice, if stereotypic, are far more severely affected than CB mice and are also more physiologically stressed and inactive than CB mice, regardless of their stereotypy status. Capturing subjects from the wild to further study these latter effects raises serious practical, ethical and potentially conservation concerns. Here, we therefore tested whether rearing CB striped mice in enriched conditions and then placing them in standard cages could provide a more suitable model for investigating how wild-caught (WC) conspecifics respond to the reduced environmental complexity they experience after capture. Compared with striped mice which were always standard-housed (n =36), enriched striped mice (n =24) were four times less likely to develop SB and, similarly to the benefits of being wild born, early environmental enrichment (30–170 days) successfully protected CB striped mice from the emergence of SB after transfer to standard caging (171–240 days). However, unlike WC mice, previously enriched CB striped mice which then became stereotypic did not develop markedly more severe SBs; they showed diverse forms, unlike stereotypic WC mice which exclusively circuit ran; and they were not more inactive once SB levels were controlled for. These findings thus show that early environmental complexity can have lasting suppressive effects on SB, suggesting that early enrichment protocols could indeed provide a practicable, potentially more ethical model for investigating the causal mechanisms underpinning birth origin effects on SB. Furthermore, they add to a corpus of data for this species showing that more naturalistic early experiences, both social and physical, lastingly protect against SB development. These results also highlight how unpredictable and poorly understood early enrichment effects are (since in some species early enrichment exacerbates later SB); and moreover reveal that early environmental complexity is not the sole factor shaping behavioural phenotypes in WC animals, with differential social experience and human contact being other likely causes of developmental divergence. [Copyright &y& Elsevier]

The behaviour and physiology of wild animals born in zoos, laboratories and breeding centres can differ substantially from that of their wild-caught (WC) conspecifics. For instance, captive-born (CB) animals are typically more prone to developing abnormal repetitive behaviours. In captive striped mice, Rhabdomys, we first confirmed that birth origin predicted the emergence of stereotypic behaviour (SB), with CB mice being most at risk. Second, to investigate correlates of this birth origin effect, we tested WC and CB striped mice in behavioural tasks to quantify fear/anxiety, activity and perseveration, and measured faecal corticosterone to assess physiological stress. WC mice proved more fearful and less active than CB animals, and had higher levels of faecal corticosterone metabolites. These effects, however, were unrelated to SB. WC mice were also less perseverative and more behaviourally flexible than CB animals, traits that covary with SB. Third, a retrospective analysis of laboratory records showed that SB incidence was significantly lower in adult-caught than juvenile-caught striped mice, with juvenile males being the most severely affected by early removal from the wild. In conclusion, our results indicate that adult, but not juvenile WC striped mice are typically protected against SB development in captivity, despite having poorer welfare than their CB conspecifics. They also reveal profound behavioural changes in CB mice, changes suggestive of altered forebrain function, a hypothesis now needing direct testing. [Copyright &y& Elsevier]

Abstract: Captive animal populations can diverge considerably from populations in the wild, despite the animals not being deliberately domesticated. If the phenotypes which are of benefit in captivity are heritable, the genotypes of captive-stock can diverge swiftly and substantially from wild-stock. Using striped mice, Rhabdomys, we tested the relationship between reproductive output and stereotypic behaviour, a heritable repetitive abnormal behaviour common in captive wild animals. Individuals (n =120; 60♂, 60♀) were assigned to pairs in one of four treatment groups formed from combinations of non-stereotypic and stereotypic mothers and fathers, and various measures of reproductive output were recorded. Reproductive output (e.g. total number of offspring) for stereotypic females (but not stereotypic males) was significantly greater than for non-stereotypic striped mice. We suggest that, overall, unintended selection is likely to increase the incidence of stereotypic behaviour in a captive striped mouse population because (1) stereotypic females breed more successfully than non-stereotypic striped mice, and (2) genetic variance underlies the trait. The potential implications of these findings for the validity of behavioural studies using captive-bred wild animals and for conservation breeding programmes are discussed. [Copyright &y& Elsevier]

Abstract: The early life experience of captive animals, in combination with their genetic inheritance, can predispose or promote the development of stereotypic behaviour in later life. To investigate the early social effects of weaning age and the presence/absence of the father on the development of stereotypic behaviour in adulthood, we retrospectively analysed data from our captive colony of striped mice, Rhabdomys. In the first analysis, pairs of young from each litter were respectively weaned on postnatal days 12 (4 days before natural weaning), 16, or 20, and the incidence of stereotypic behaviour recorded between days 50 and 60. Early weaning (day 12) was associated with a significantly higher incidence of stereotypic behaviour than later weaning (day 16 or 20). In the second analysis, pups were raised with either the father present (biparental care) or absent (uniparental care). Biparentally reared animals showed significantly less stereotypic behaviour as adults than individuals reared by their mother alone. In both analyses, young from stereotypic mothers showed a higher incidence of stereotypic behaviour than offspring from non-stereotypic dams, with experiential and genetic effects combining to influence the adult phenotype. Together, these data indicate that the early social environment influences the development of stereotypic behaviour in adulthood, and suggest directions for future research into the mechanisms of the epigenetic effects of early social experience on the development of stereotypic behaviour, such as whether amounts of parental care received per pup cause these effects, and whether changes in stereotypic behaviour are paralleled by changes in stress responsiveness. [Copyright &y& Elsevier]

Abstract: Environmentally induced stereotypy is the most common abnormal behaviour in captive animals. However, not all animals housed in identically impoverished environments develop stereotypy, possibly because of differences in genetic predisposition. To investigate the transmission of stereotypy in striped mice, Rhabdomys, we established four breeding treatments (non-stereotypic parents; stereotypic mother and non-stereotypic father; non-stereotypic mother and stereotypic father; stereotypic parents), and recorded offspring stereotypy prevalence. The prevalence of stereotypy was five times greater in the offspring of stereotypic than those of non-stereotypic females, regardless of whether the sire was stereotypic, and three times greater in offspring sired by stereotypic males paired with non-stereotypic females than in offspring from non-stereotypic parents. Our data show that stereotypy has a strong genetic component. However, the greater maternal than paternal contribution to stereotypy prevalence in offspring indicates that genetics alone cannot explain the observed transmission pattern. As previous work has excluded social influences on the development of stereotypy, we suggest that maternally mediated prenatal factors (e.g. gestational stress) might also predispose the stereotypic phenotype in striped mice. [Copyright &y& Elsevier]