Evidence for Adaptation to the Tibetan Plateau Inferred from Tibetan Loach Transcriptomes

Abstract

Triplophysa fishes are the primary component of the fish fauna on the Tibetan Plateau and are well adapted to the high-altitude environment. Despite the importance of Triplophysa fishes on the plateau, the genetic mechanisms of the adaptations of these fishes to this high-altitude environment remain poorly understood. In this study, we generated the transcriptome sequences for three Triplophysa fishes, that is, Triplophysa siluroides, Triplophysa scleroptera, and Triplophysa dalaica, and used these and the previously available transcriptome and genome sequences from fishes living at low altitudes to identify potential genetic mechanisms for the high-altitude adaptations in Triplophysa fishes. An analysis of 2,269 orthologous genes among cave fish (Astyanax mexicanus), zebrafish (Danio rerio), large-scale loach (Paramisgurnus dabryanus), and Triplophysa fishes revealed that each of the terminal branches of the Triplophysa fishes had a significantly higher ratio of nonsynonymous to synonymous substitutions than that of the branches of the fishes from low altitudes, which provided consistent evidence for genome-wide rapid evolution in the Triplophysa genus. Many of the GO (Gene Ontology) categories associated with energy metabolism and hypoxia response exhibited accelerated evolution in the Triplophysa fishes compared with the large-scale loach. The genes that exhibited signs of positive selection and rapid evolution in the Triplophysa fishes were also significantly enriched in energy metabolism and hypoxia response categories. Our analysis identified widespread Triplophysa-specific nonsynonymous mutations in the fast evolving genes and positively selected genes. Moreover, we detected significant evidence of positive selection in the HIF (hypoxia-inducible factor)-1A and HIF-2B genes in Triplophysa fishes and found that the Triplophysa-specific nonsynonymous mutations in the HIF-1A and HIF-2B genes were associated with functional changes. Overall, our study provides new insights into the adaptations and evolution of fishes in the high-altitude environment of the Tibetan Plateau and complements previous findings on the adaptations of mammals and birds to high altitudes.

Selection of reference genes for qRT‐PCR and expression analysis of high‐altitude‐related genes in grassland caterpillars (Lepidoptera: Erebidae: Gynaephora) along an altitude gradient

“…The expression responses of GPI to divergent altitudes might be key in the adaptation of the energy metabolism of TP Gynaephora species. HIF1A is a main regulator in the hypoxia signaling pathway, and responses to hypoxia are largely regulated by changes in its expression in other animals (Wang et al., 2015; Xiao, 2015). Here, we observed significant expression changes in HIF1A along an altitudinal gradient, suggesting that the expression of this gene may be associated with adaptation to hypoxia in Gynaephora .…”

Comprehensive Transcriptome Analysis Provides Evidence of Local Thermal Adaptation in Three Loaches (Genus: Misgurnus)

“…Since the development of next-generation sequencing technology, RNA-seq has been widely used as an efficient and accessible approach to determine the evolutionary histories of non-model organisms when no genome information is available [28,29,30]. Here, we sequenced and assembled the transcriptomes of three closely related Misgurnus species, M. anguillicaudatus , M. bipartitus , and M. mohoity , to identify the genetic mechanisms in their adaptation to the temperature variations in their environments and provide valuable information for further studies to understand the genetic makeup of other fishes in thermal adaptations.…”

“…If the p value was < 0.05, and a higher Ka/Ks (the ratio of nonsynonymous to synonymous Substitutions) value was obtained than the foreground branch than the background branches, the gene was considered to be a fast-evolving gene. To identify genes under positive selection, the branch-site model in the codeml program was used, with the null model assuming that all branches have been evolving at the same rate and the alternative model allowing foreground branch to evolve under a different rate [29,30]. As before, LRTs were used to discriminate between alternative models for each gene in the gene set, and p value was computed by comparing LRT to the χ 2 distribution, with the degree of freedom estimated as the difference of parameters between models.…”

Regulatory architecture of gene expression variation in the threespine stickleback, Gasterosteus aculeatus

“…Thus, HIF1A is of relevance when fish colonize aquatic environments with differing oxygen regimens, for example benthic vs. limnetic habitats or different areas of the Baltic Sea. Rytkönen et al (2007) found no association between variation in the HIF1A coding region and adaptation to hypoxic conditions across various fish species, and markers linked to HIF1A do not appear be under directional selection among Baltic Sea stickleback populations ; however, the gene was recently found to be under positive selection in high-altitude loach lineages (Wang et al 2015). HIF1A is known to be transcriptionally regulated in fish (Liu et al 2013), and our identification of a trans-eQTL for HIF1A demonstrates that regulatory variation for this gene is present in Baltic Sea sticklebacks and could be an alternative, unexamined, target of selection.…”