Evolution of gene expression across brain regions in behaviourally divergent deer mice

Abstract

The evolution of innate behaviours is ultimately due to genetic variation likely acting in the nervous system. Gene regulation may be particularly important because it can evolve in a modular brain‐region specific fashion through the concerted action of cis‐ and trans‐regulatory changes. Here, to investigate transcriptional variation and its regulatory basis across the brain, we perform RNA sequencing (RNA‐Seq) on ten brain subregions in two sister species of deer mice (Peromyscus maniculatus and P. polionotus)—which differ in a range of innate behaviours, including their social system—and their F1 hybrids. We find that most of the variation in gene expression distinguishes subregions, followed by species. Interspecific differential expression (DE) is pervasive (52–59% of expressed genes), whereas the number of DE genes between sexes is modest overall (~3%). Interestingly, the identity of DE genes varies considerably across brain regions. Much of this modularity is due to cis‐regulatory divergence, and while 43% of genes were consistently assigned to the same gene regulatory class across subregions (e.g. conserved, cis‐ or trans‐regulatory divergence), a similar number were assigned to two or more different gene regulatory classes. Together, these results highlight the modularity of gene expression differences and divergence in the brain, which may be key to explain how the evolution of brain gene expression can contribute to the astonishing diversity of animal behaviours.

Timing-dependent effects of elevated maternal glucocorticoids on offspring brain gene expression in a wild small mammal

“…Because we expected baseline differences between brain regions (e.g. Kautt et al, 2024; Nadler et al, 2006), regardless of treatment group, we used Trinity (v2.15.1; Grabherr et al, 2011; Haas et al, 2013) to assemble separate transcriptomes for the hypothalamus and hippocampus. We then used CD-HIT-EST from the program CD-HIT (v4.8.1; Fu et al, 2012; Li & Godzik, 2006) to cluster overlapping contigs and removed any contigs <250bp long.…”