Chromosomal genome of Triplophysa bleekeri provides insights into its evolution and environmental adaptation

Abstract

Background: Intense stresses caused by high-altitude environments may result in noticeable genetic adaptions in native species. Studies of genetic adaptations to high elevations have been largely limited to terrestrial animals. How fish adapt to high-elevation environments is largely unknown. Triplophysa bleekeri, an endemic fish inhabiting high-altitude regions, is an excellent model to investigate the genetic mechanisms of adaptation to the local environment. Here, we assembled a chromosomal genome sequence of T. bleekeri, with a size of ∼628 Mb (contig and scaffold N50 of 3.1 and 22.9 Mb, respectively). We investigated the origin and environmental adaptation of T. bleekeri based on 21,198 protein-coding genes in the genome.

Results: Compared with fish species living at low altitudes, gene families associated with lipid metabolism and immune response were significantly expanded in the T. bleekeri genome. Genes involved in DNA repair exhibit positive selection for T. bleekeri, Triplophysa siluroides, and Triplophysa tibetana, indicating that adaptive convergence in Triplophysa species occurred at the positively selected genes. We also analyzed whole-genome variants among samples from 3 populations. The results showed that populations separated by geological and artificial barriers exhibited obvious differences in genetic structures, indicating that gene flow is restricted between populations.

Conclusions: These results will help us expand our understanding of environmental adaptation and genetic diversity of T. bleekeri and provide valuable genetic resources for future studies on the evolution and conservation of high-altitude fish species such as T. bleekeri.

Keywords: Triplophysa bleekeri; genetic adaptation; genome; population genomics.

Figure 1:

Morphology and geographic distribution of T. bleekeri. (a) T. bleekeri used in this study. (b) Geographic distribution of the sampling locations for T. bleekeri. The red circles, green triangle, yellow trapezoid, and dotted ellipse represent the sampling sites, gorge, artificial dam, and Wuxi Town, respectively.

Figure 2:

Phylogenetic relationships and divergence time estimation for T. bleekeri and other fish species. All nodes were completed and supported by 100 cycles of bootstrap resampling. Numbers near the nodes (shown in blue) indicate the estimated divergence times with a 95% confidence interval. Divergences used for the recalibration of time estimation are indicated with red dots.

Figure 3:

Natural positively selected gene (PSG) identification and functional analysis for T. bleekeri, T. tibetana, and T. siluroides. (a) Venn diagram for PSGs for the 3 fish species. (b) Venn diagram for PSs identified from species- and lineage-based method. (c) Enrichment analysis on the biological pathways for candidate PSGs identified from the species- and lineage-based method. mRNA: messenger RNA.

Figure 4:

Historical effective population size profile deduced from the whole-genome sequencing data. One hundred bootstrap replicates were performed for the effective population size estimation.

Figure 5:

Population genetics analysis for T. bleekeri. (a) Neighbor-joining phylogenetic tree of individuals based on whole-genome SNP loci. Samples from population LHK, XX, and BY are labeled with red, green and blue, respectively. (b) Principal component (PC) analysis plots of the first 2 components. The fraction of the variance obtained was 14.5% for PC1 and 6.4% for PC2. (c) Population structure plots of T. bleekeri. The samples from population LHK, XX, and BY are represented by red, green, and blue color, respectively. We assume that there were 3 populations for the analysis (K = 3). The y axis quantifies the proportion of the individual's genome from inferred ancestral populations, and x axis shows the different populations.

Figure 6:

Selective sweep analysis to identify candidate selected functional genes among populations. (a) Manhattan plot to show the genome-wide differentiation between LHK and BY populations. (b) Venn plot for shared enriched biological pathway for candidate selected functional genes from the selective sweep analysis among population comparisons. (c) The shared enriched biological pathway from LHK-BY and XX-BY comparisons. (d) The Fst profiles for genomic regions containing treh, ctnnb1, and lef1 genes.