Population Genomic Analysis of Two Endemic Schizothoracins Reveals Their Genetic Differences and Underlying Selection Associated with Altitude and Temperature

SIMPLE SUMMARY: Diptychus maculates and Gymnodiptychus dybowskii are two rare aboriginal fishes in the Xinjiang Uygur Autonomous Region. In recent years, due to overfishing and habitat fragmentation caused by construction of water conservancy and hydropower projects, the fishery resources have decreased sharply. Understanding the genetic background is of great significance for resource protection. In this study, we revealed the similar trends of population genetic diversities in these two species collected from the Tarim River and the Yili River. In addition, outlier SNPs associated with temperature and altitude were detected in both of them, indicating that Schizothoracinae fishes represented by D. maculates and G. dybowskii were still under the selection pressure of plateau environments. ABSTRACT: Schizothoracins are a group of cyprinid fishes distributed throughout the Qinghai–Tibet Plateau, which can be classified in three grades: primitive, specialised and highly specialised according to adaptation ability to plateau environments. As the only specialised schizothoracins in Xinjiang, China, Diptychus maculates and Gymnodiptychus dybowskii are ideal materials for adaptive evolution research. Based on single-nucleotide polymorphism (SNP) loci detected by specific-locus amplified fragment (SLAF) technology, the genome-wide genetic diversities of these two species from nine sites in Xinjiang were evaluated. D.maculates in the Muzat River (BM) and G. dybowskii in the Kaidu River (LKG) presented the lowest genetic diversity levels, whereas D. maculates in the Kumarik River (BK) and G.dybowskii in the Kashi River (LK) were just the opposite. Cluster and principal component analysis demonstrated a distant genetic affinity between D. maculates in the Tashkurgan River (BT) and other populations. Outlier SNP loci were discovered both in D. maculates and G. dybowskii. The coalescent Bayenv and latent factor mixed model (LFMM) methods showed that a total of thirteen and eighteen SNPs in D. maculates were associated with altitude and temperature gradient, respectively. No intersection was revealed in G. dybowskii. The results indicated that D. maculates was subject to much greater divergent selection pressure. A strong signal of isolation-by-distance (IBD) was detected across D. maculates (Mantel test, rs = 0.65; p = 0.05), indicating an evident geographical isolation in the Tarim River. Isolation-by-environment (IBE) analysis implied that temperature and altitude selections were more intensive in D. maculates, with greater environmental variation resulting in weak gene flow.