brain

Sorex araneus, the Eurasian common shrew, has seasonal brain size plasticity (Dehnel’s phenomenon) and abundant intraspecific chromosomal rearrangements, but genomic contributions to these traits remain unknown. We couple a chromosome-scale genome assembly with seasonal brain transcriptomes to discover relationships between molecular changes and both traits. Positively selected genes enriched the Fanconi anemia DNA repair pathway, which prevents the accumulation of chromosomal aberrations, and is likely involved in chromosomal rearrangements (FANCI, FAAP100). Genes involved in neurogenesis show either signatures of positive selection (PCDHA6), seasonal differential expression in the cortex and hippocampus (Notch signaling), or both (SOX9), suggesting a role for cellular proliferation in seasonal brain shrinkage and regrowth. Both positive selection and evolutionary upregulation in the shrew hypothalamus of VEGFA and SPHK2 indicate adaptations in hypothalamic metabolic homeostasis have evolved together with Dehnel’s phenomenon. These findings reveal genomic changes central to the evolution of both chromosomal instability and cyclical patterns in brain gene expression that characterizes mammalian brain size plasticity.

Captivity, frequently used in animal research, can profoundly alter brain size, cognitive abilities and activity levels. Critically, persistent exposure to stressors in captive environments can lead to chronic stress and subsequently to a range of health issues. However, the direct implications of captivity on research outcomes have not been thoroughly investigated. We examined the effects of captivity on the common shrew, Sorex araneus, a species that exhibits a profound seasonal reversible change in brain and body size. We compared wild shrews during summer and winter to assess seasonal changes in brain size and behaviour and then contrasted these findings with shrews kept in captivity for six months. Using repeated in vivo magnitic resonance imaging, we determined that the extent of seasonal brain size change was not affected by the semi-natural captive conditions. However, captivity led to increased activity levels and reduced learning motivation in the shrews, indicative of chronic stress. These results suggest that even semi-natural conditions can significantly alter the outcome of studies and these effects need to be quantified before experimentation.

Compared with their free-ranging counterparts, wild animals in captivity experience different conditions with lasting physiological and behavioural effects. Although shifts in gene expression are expected to occur upstream of these phenotypes, we found no previous gene expression comparisons of captive versus free-ranging mammals. We assessed gene expression profiles of three brain regions (cortex, olfactory bulb and hippocampus) of wild shrews (Sorex araneus) compared with shrews kept in captivity for two months and undertook sample dropout to examine robustness given limited sample sizes. Consistent with captivity effects, we found hundreds of differentially expressed genes in all three brain regions, 104 overlapping across all three, that enriched pathways associated with neurodegenerative disease, oxidative phosphorylation and genes encoding ribosomal proteins. In the shrew, transcriptomic changes detected under captivity resemble responses in several human pathologies, including major depressive disorder and neurodegeneration. While interpretations of individual genes are tempered by small sample sizes, we propose captivity influences brain gene expression and function and can confound analyses of natural processes in wild individuals under captive conditions.