How voles adapt to subterranean lifestyle: Insights from RNA-seq

Abstract

Life under the earth surface is highly challenging and associated with a number of morphological, physiological and behavioral modifications. Subterranean niche protects animals from predators, fluctuations in environmental parameters, but is characterized by high levels of carbon dioxide and low levels of oxygen and implies high energy requirements associated with burrowing. Moreover, it lacks most of the sensory inputs available above ground. The current study describes results from RNA-seq analysis of four subterranean voles from subfamily Arvicolinae:Prometheomys schaposchnikowi,Ellobius lutescens,Terricola subterraneus, andLasiopodomys mandarinus. Original RNA-seq data were obtained for eight species, for nine species, SRA data were downloaded from the NCBI SRA database. Additionally assembled transcriptomes of Mynomes ochrogaster and Cricetulus griseus were included in the analysis. We searched for the selection signatures and parallel amino acid substitutions in a total of 19 species. Even within this limited data set, we found significant changes ofdN/dSratio by free-ratio model analysis for subterranean Arvicolinae. Parallel substitutions were detected in genesRAD23BandPYCR2. These genes are associated with DNA repair processes and response to oxidative stress. Similar substitutions were discovered in theRAD23genes for highly specialized subterraneanHeterocephalus glaberandFukomys damarensis. The most pronounced signatures of adaptive evolution related to subterranean niche within species of Arvicolinae subfamily were detected forEllobius lutescens. Our results suggest that genomic adaptations can occur very quickly so far as the amount of selection signatures was found to be compliant with the degree of specialization to the subterranean niche and independent from the evolutionary age of the taxon. We found that the number of genomic signatures of selection does not depend on the age of the taxon, but is positively correlated with the degree of specialization to the subterranean niche.