Coordinated shifts in gene expression and regulation identify fast evolving loci linked to unique mole-rat traits

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Abstract Background Changes in gene expression regulation are central to the acquisition of novel phenotypes during mammalian evolution. However, transcriptomes substantially accumulate neutral divergence over evolutionary time. As a result, selection-driven gene expression shifts are difficult to distinguish from neutral changes, thereby blurring adaptive signatures during genome evolution. Here, we integrate comparative multiomics data within a phylogeny-aware framework of quantitative trait evolution to jointly investigate how gene expression and regulation have evolved in African mole-rats. This group of rodents displays striking physiological adaptations to subterranean life; how those adaptations are encoded in their genomes remains poorly characterised. Results Using RNA-seq from liver and heart in two mole-rat species and two rodent outgroups, we reliably identify hundreds of genes whose expression levels have experienced lineage-specific accelerated evolution consistent with selection rather than drift. To connect expression evolution with regulatory mechanisms, we integrate this transcriptome data with epigenomic profiles of cis-regulatory landscapes, which experience high turnover in mammalian evolution. Conclusions Our results demonstrate that genes with lineage-specific expression shifts are surrounded by epigenomic landscapes that also display signals of accelerated evolution, providing support for selection over genomic processes diverging at different rates. Our approach illuminates how gene regulation and expression evolve in concert in this mammalian model and highlights genomic loci with concordant evidence for phenotypic adaptation. The molecular signatures we observe reveal selective pressures acting on key pathways for mole-rat physiology, including metabolism and stress responses.

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