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

Abstract

Sorex araneus, the Eurasian common shrew, has seasonal brain size plasticity (Dehnel's phenomenon) and many intraspecific chromosomal rearrangements. Genomic contributions to these traits, however, remain unknown. We couple a chromosome-scale genome assembly with seasonal brain transcriptomes to discover relationships between molecular evolution and both traits. While Positively Selected Genes (PSGs) enriched the Fanconi anemia DNA repair pathway (FANCI, FAAP100), which is likely involved in chromosomal rearrangements by preventing the accumulation of chromosomal aberrations, genes under positive selection or showing seasonal differential expression in the brain implicate neurogenesis (PCDHA6, SOX9, Notch signaling) and metabolic regulation (VEGFA, SPHK2) as key mechanisms underlying Dehnel's phenomenon. We also find that both positively selected and differentially expressed genes in the hippocampus are overrepresented near S. araneus evolutionary breakpoints. This relates both positive selection and differential expression to accessible chromatin configuration, suggesting that chromosomal rearrangements are integral to adaptive evolution and the regulation of brain size plasticity.