Transcriptomic signature of rapidly evolving immune genes in a highland fish

Abstract

Recent genome-wide studies have begun to elucidate the genomic basis of hypoxia, long-term cold and high saline and alkaline adaptation in highland fish, and a number of key genes contributed to its highland adaptation were identified. An increasing number of studies indicated that immune genes of Tibetan endemic fish species underwent positive selection towards functional shift, while the insight into immune gene repertoire of Tibetan highland fishes from genome-wide studies has largely lagged behind. In this study, we performed one of the first comparative genomics study in particular focusing on the signatures of immune genes in a highland fish, Gymnocypris przewalskii based on immune-relevant tissue transcriptome assemblies. We identified seven putative rapidly evolving immune genes with elevated molecular evolutionary rate (dN/dS) relative to lowland fish species. Using tissue-transcriptome data, we found most of rapidly evolving immune genes were broadly expressed in head-kidney, spleen, gills and skin tissues, which significantly enriched for complement activation and inflammatory response processes. In addition, we found a set of complement activation related genes underwent accelerated evolution and showed consistently repressed expression patterns in response to parasite Ichthyophthirius multifiliis infection. Moreover, we detected a number of immune genes involved in adaptive immune system exhibited distinct signature of upregulated expression patterns after parasite infection. Taken together, this study provided putative transcriptomic signatures of rapidly evolving immune genes, and will gain the insight into Schizothoracine fish adaptation to high-altitude extreme aquatic environments including diversified pathogen challenge.