Certain complex phenotypes appear repeatedly across diverse species due to processes of evolutionary conservation and convergence. In some contexts like developmental body patterning, there is increased appreciation that common molecular mechanisms underlie common phenotypes; these molecular mechanisms include highly conserved genes and networks that may be modified by lineage-specific mutations. However, the existence of deeply conserved mechanisms for social behaviors has not yet been demonstrated. We used a comparative genomics approach to determine whether shared neuromolecular mechanisms could underlie behavioral response to territory intrusion across species spanning a broad phylogenetic range: house mouse (Mus musculus), stickleback fish (Gasterosteus aculeatus), and honey bee (Apis mellifera). Territory intrusion modulated similar brain functional processes in each species, including those associated with hormone-mediated signal transduction and neurodevelopment. Changes in chromosome organization and energy metabolism appear to be core, conserved processes involved in the response to territory intrusion. We also found that several homologous transcription factors that are typically associated with neural development were modulated across all three species, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. Furthermore, immunohistochemical analyses of a subset of these transcription factors in mouse again implicated modulation of energy metabolism in the behavioral response. These results provide support for conserved genetic "toolkits" that are used in independent evolutions of the response to social challenge in diverse taxa.genetic hotspot | NF-κB signaling | brain metabolism | aggression S imilar phenotypes can have a shared molecular basis, even among distantly related species (1-3). This phenomenon has been observed for an array of traits, including morphological adaptations like coat color or wing patterning, rapid adaptations like drug resistance, and artificially selected phenological traits like flowering time (reviewed in ref. 2). Shared molecular mechanisms can arise convergently as a result of de novo mutations at genetic hotspots (2) or as a result of conservation. Both of these processes result in "genetic toolkits" or genes that are repeatedly used over evolutionary time to give rise to similar phenotypes (3). The phenomenon of genetic toolkits challenges fundamental notions about evolutionary convergence, conservation, and the origins of biodiversity.The role of genetic toolkits in shaping behavioral phenotypes is unclear (4, 5). Behaviors are typically polygenic (6) and they show great nuance and plasticity within a species, raising the possibility that cross-species similarities in behavior are superficial. Social behaviors in particular present a challenge to the genetic toolkit concept: these behaviors are critical to survival and reproductive success, but across species there is significant variation in the contexts for an...

Coping strategies have been associated with differential stress responsivity, perhaps providing a valuable neurobiological marker for susceptibility to the emergence of depressogenic symptoms or vulnerability to other anxiety-related disorders. Rats profiled with a flexible coping phenotype, for example, exhibit increased neurobiological markers of emotional regulation compared to active and passive copers (Bardi et al., 2012; Lambert et al., 2014). In the current study, responses of male and female rats to prediction errors in a spatial foraging task (dry land maze; DLM) were examined after animals were exposed to chronic unpredictable stress (CUS). Brains were processed following the DLM training/assessment for fos-activation patterns and several measures of neuroplasticity in relevant areas. Behavioral responses observed during both the CUS and DLM phases of testing suggested that males and females employ different means of gathering information such as increased ambulatory exploration in males and rear responses in females. Fecal samples collected during baseline and following CUS swim exposure revealed higher corticosterone (CORT) in active copers, whereas flexible copers had higher dehydroepiandrosterone (DHEA) and DHEA/CORT ratios, both indications of enhanced emotional regulation. Focusing on the neural analysis, flexible copers exhibited fewer fos-immunoreactive cells in the basolateral amygdala and a trend toward lower activation in the insula while encountering the prediction error associated with the DLM probe trial. Coping profiles also differentially influenced markers of neuroplasticity; specifically, flexible copers exhibited higher levels nestin-immunoreactivity (ir). Further, less hippocampal glucocorticoid receptor-ir was observed in the flexible copers than the active and passive copers. In sum, flexible coping rats exhibited evidence of emotional resilience as indicated by several neurobiological measures; however, despite increased rates of depression and related symptoms reported in human females, sex effects weren’t as pervasive as coping strategy profiles in the analysis of neurobiological markers employed in the current study.

Both social and physical stimuli contribute to the complexity of an animal’s environment, influencing biobehavioral responses to subsequent challenges. In the current study, male Long-Evans rats were randomly assigned to an isolate (ISO), social control (SC) or social enriched (SE) group (n = 8 per group). The SC and SE conditions were group housed with the SE group exposed to physical enrichment stimuli that were natural as opposed to manufactured (e.g., hollowed out log instead of plastic hiding place). On three occasions during their 40-day enriched environment exposure, night/dark phase videos were obtained for 1 h during the early part of the dark phase. During this time, the SE animals exhibited significantly more social grooming with no differences between the SE and SC in the frequency of play or self-grooming bouts. Subsequently, all animals were assessed in social interaction and problem-solving escape tasks during the last week of the enriched environment exposure. SE rats exhibited increased digging bouts toward the restrained conspecific in the social interaction task whereas the other groups exhibited more escape responses. In the problem-solving task, SE animals exhibited a decreased latency to cross the barrier to escape from the predator odor (i.e., cat urine and fur). Neural analyses indicated increased oxytocin-immunoreactive (OT-ir) tissue in the SE supraoptic and paraventricular nuclei of the hypothalamus compared to the other groups. Interestingly, blood samples indicated lower peripheral corticosterone (CORT) and higher OT levels in the ISO animals when compared to the SC and SE animals, an effect retrospectively attributed to separation anxiety in the SE and SC animals in preparation for histology procedures. When the behavioral, neural and endocrine data were visualized as a multifaceted dataset via a multidimensional scaling analysis, however, an association between social enrichment and higher OT involvement was observed in the SE animals, as well as heightened stress responsivity in the ISO and SC groups. In sum, the SE animals exhibited a facilitation of social responses, problem-solving ability and OT immunoreactive responsiveness. These findings provide new information about the influences of both physical and social stimuli in dynamic and enriched environments.

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