Abstract
BackgroundAppropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care. Many studies shedding light on the neurobiological underpinnings of social behavior have focused on nonapeptides (vasopressin, oxytocin, and homologues) and on sexual or parent-offspring interactions. Furthermore, animals have been studied under artificial laboratory conditions, where the consequences of behavioral responses may not be as critical as when expressed under natural environments, therefore obscuring certain physiological responses. We used automated recording of social interactions of wild house mice outside of the breeding season to detect individuals at both tails of a distribution of egocentric network sizes (characterized by number of different partners encountered per day). We then used RNA-seq to perform an unbiased assessment of neural differences in gene expression in the prefrontal cortex, the hippocampus and the hypothalamus between these mice with naturally occurring extreme differences in social network size.ResultsWe found that the neurogenomic pathways associated with having extreme social network sizes differed between the sexes. In females, hundreds of genes were differentially expressed between animals with small and large social network sizes, whereas in males very few were. In males, X-chromosome inactivation pathways in the prefrontal cortex were the ones that better differentiated animals with small from those with large social network sizes animals. In females, animals with small network size showed up-regulation of dopaminergic production and transport pathways in the hypothalamus. Additionally, in females, extracellular matrix deposition on hippocampal neurons was higher in individuals with small relative to large social network size.ConclusionsStudying neural substrates of natural variation in social behavior in traditional model organisms in their habitat can open new targets of research for understanding variation in social behavior in other taxa.
Highlights
Appropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care
We usually study the neurobiology of mammalian social behavior in somewhat simplified settings, using inbred animals, housed in conditions that are likely to prevent them from displaying their natural repertoire of behavioral and physiological responses [18]
To obtain animals with contrasting social network sizes, we sampled individuals at both tails of a distribution of egocentric social network size for the population during the non-breeding season
Summary
Appropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care. Animals are presented with an environment where the consequences of behavioral and physiological responses for survival may not be as severe as in a natural environment; the level of sterility and standardization may obscure certain responses (e.g., [19, 20]) or not apply to even slight deviations of the environmental conditions tested [21, 22]. This has important implications for the translational value that animal models have for neuropsychiatric disorders [23]. The challenge here is that many animals are difficult to observe in the wild, making detailed behavioral quantifications impractical
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