Genomic comparisons shed light on the adaptive basis of brain size plasticity and chromosomal instability in the Eurasian common shrew

Sorex araneus, the Eurasian common shrew, has seasonal brain size plasticity (Dehnels 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 Dehnels 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. TeaserGenomic and expression variations are key to chromosomal instability and seasonal brain plasticity in the common shrew.