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MATERIALS and METHODS the Complete Mitochondrial Genome Sequences of Schizothoracinae and Its Relatives Within the Cypriniformes

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MATERIALS and METHODS the Complete Mitochondrial Genome Sequences of Schizothoracinae and Its Relatives Within the Cypriniformes MATERIALS AND METHODS search among the 15 possible tree topologies for four clades (Morphologically Specialized Schizothoracinae, The complete mitochondrial genome sequences of Morphologically Primitive Schizothoracinae, Barbinae Schizothoracinae and its relatives within the Cypriniformes sensu stricto and Barbinae sensu lato). The phylogenetic were retrieved from NCBI; their accession numbers are relationships within each clade as well as within the out- shown in Fig. 1 and Supplementary Fig. S1. The 12 pro- group (Cyprininae and Barbinae sensu lato except for tein-coding genes encoded in the H strand and two ribo- Spinibarbus) were fixed in advance in accordance with somal RNA genes were separately aligned by the the ML tree topology inferred by the RAxML program MUSCLE program (Edgar, 2004). Alignments were (Supplementary Fig. S1). The mtREV24F+Γ and GTR+Γ checked by eye and all ambiguously aligned sites were models were used for the protein-coding genes and rRNA excluded. Start and stop codons as well as the overlap- genes, respectively. Statistical tests were done using the ping regions between genes were also excluded. The CONSEL program (Shimodaira and Hasegawa, 2001). protein-coding genes and rRNAs were concatenated. Positively selected sites along specific branches were Phylogenetic trees were inferred by the RAxML program detected with the branch site model (Yang and Nielsen, ver. 7.7.1 (Stamatakis et al., 2008) using the 2002) using CODEML. We also applied a site model that mtREV24F+I+Γ model (for the protein-coding genes) and allows heterogeneity of the ω ratios among sites to detect the GTR+I+Γ model (for rRNAs). The CODEML and positively selected sites (Nielsen and Yang, 1998; Yang, BASEML programs of PAML ver. 4.7 (Yang, 2007) were 2000); CODEML was also used for this analysis. Posi- also used for phylogenetic inference with an exhaustive tively selected codon sites were predicted by the Bayes Schizopygopsis thermalis KC558499 㻝㻜㻜 Gymnocypris namensis KC558498 Gymnocypris dobula KC558497 㻝㻜㻜 㻝㻜㻜 Schizopygopsis younghusbandi JX232379 㻝㻜㻜 Gymnocypris przewalskii AB239595 㻝㻜㻜 Gymnocypris eckloni JQ004279 㻝㻜㻜 Oxygymnocypris stewartii KF528985 㻝㻜㻜 Ptychobarbus dipogon KF597526 㻥㻜 Gymnodiptychus pachycheilus KF976395 Barbus barbus AB238965 㻝㻜㻜 Luciobarbus capito JX987313 㻝㻜㻜 Schizothorax dolichonema KJ184546 Schizothorax prenanti KJ126773 㻟㻣 㻡㻜 Schizothorax richardsonii KC790369 㻤㻟 Schizothorax labiatus KF739398 㻝㻜㻜 Schizothorax esocinus KF600713 Schizothorax progastus KF739399 㻝㻜㻜 㻝㻜㻜 Schizothorax wangchiachii KC292197 㻢㻞 Schizothorax oconnori KC513575 㻝㻜㻜 㻝㻜㻜 Schizothorax waltoni JX202592 Schizothorax macropogon KC020113 㻝㻜㻜 㻡㻡 Aspiorhynchus laticeps KF564793 㻝㻜㻜 Schizothorax biddulphi JQ844133 㻡㻝 Schizothorax plagiostomus KF928796 㻝㻜㻜 Spinibarbus caldwelli KF134718 Spinibarbus denticulatus KC852197 㻝㻜㻜 Spinibarbus sinensis KC579368 㻤㻣 Cyprinus carpio AP009047 㻤㻡 Carassius auratus AB006953 㻥㻥 Barbonymus schwanenfeldii KJ573467 Barbonymus gonionotus AB238966 㻝㻜㻜 Puntius snyderi KC113210 㻝㻜㻜 Puntius semifasciolatus KC113209 㻤㻡 Barbus trimaculatus AB239600 Pethia ticto AB238969 㻝㻜㻜 Puntius chalakkudiensis JX311437 㻝㻜㻜 Puntius denisonii KF019637 㻤㻥 Systomus tetrazona EU287909 Hemibarbus barbus AB070241 㻜㻚㻜㻝 Supplementary Fig. S1. The ML tree as inferred from the mitochondrial genomes is shown. The branch lengths are proportional to the numbers of amino acid (for 12 protein-coding genes) and nucleotide (12S rRNA and 16S rRNA) substitutions. The nodal numbers are the bootstrap probabilities (rapid bootstrap algorithm: 100 replications). The scale bar shows the number of substitutions per site. Empirical Bayes method (Yang et al., 2005). With the aim of addressing this issue, we subjected this Protein secondary structures were predicted by the clade to an extensive branch site model analysis. Thir- SOSUI engine ver. 1.11 program (http://harrier.nagahama- teen species of this clade were used (a total of 23 branches i-bio.ac.jp/sosui/), using the mitochondrial gene sequence were analyzed one by one). The tree topology was fixed data of Aspiorhynchus laticeps (KF564793). Ancestral in accordance with the ML tree topology (Fig. 1, Supple- states of the amino acid sequences were inferred by the mentary Fig. S1) for this analysis. Positive selection was ML method (Yang et al., 1995) with the mtREV24F model detected in four branches (Schizothorax labiatus, S. (Adachi and Hasegawa, 1996) using CODEML. richardsonii, S. plagiostomus and A. laticeps: Fig. 1, Sup- plementary Table S2). The ω ratios of the positively RESULTS AND DISCUSSION selected sites in all four of these branches are signifi- cantly greater than 1 (P-value of the LRT < 0.01). These Detection of recent positive selection (after the branches are all terminal branches, and their evolution- Late Miocene) In this study, we failed to detect posi- ary histories are young (after the Late Miocene; Li et al., tively selected sites in the ancestral branch of the mor- 2013). Li et al. (2013) reconstructed the ancestral geo- phologically primitive Schizothoracinae. This probably graphic distribution areas of the Schizothoracinae and reflects a low degree of high-altitude adaptation in mem- their relatives using the phylogenetic concept, and sug- bers of this clade due to lower-altitude distribution (1500– gested that the morphologically primitive clade migrated 2500 m) as well as their relatively recent migration to the to the QTP during the Late Miocene to Pleistocene. The QPT (see main text). However, the morphologically timing of positive selection in this clade is consistent with primitive Schizothoracinae may now be undergoing posi- the timing of this proposed migration to the QTP, and tive selection, because positive selection in particular lin- members of this clade may thus now be in the process of eages could be observed. high-altitude adaptation. Supplementary Table S1. Candidates for positively selected sites and their amino acid substitution pattern in the ancestral branches of the morphologically specialized clade Gene Site1 Substuon 2 PP3 Secondary Structure4 Branch5 30 Ile --> Cys 0.836 Loop region branch2 ATP6 81 Ile --> Val 0.715 Transmembrane branch3 16 Asp --> Ser 0.539 Loop region branch1 cytb 159 Met --> Val 0.508 Transmembrane branch1 192 Ala --> Met 0.692 Transmembrane branch3 8 Ile --> Ala 0.939 Loop region branch2 99 Met --> Ala 0.735 Transmembrane branch2 125 Leu --> Thr 0.774 Transmembrane branch7 NADH2 145 Thr --> Val 0.935 Loop region branch2 191 Ile --> Val 0.558 Transmembrane branch1 271 Thr --> Ser 0.552 Loop region branch1 NADH3 3 Val --> Ile 0.592 Loop region branch7 NADH4 389 Asn --> Gly 0.884 Transmembrane branch1 35 Glu --> Ser 0.927 Loop region branch7 55 Ile --> Val 0.572 Transmembrane branch1 78 Val --> Ile 0.580 Loop region branch1 NADH5 544 Leu --> Ala 0.918 Loop region branch1 579 Val --> Thr 0.548 Loop region branch7 581 Asn --> Gly 0.928 Loop region branch2 1 Posively selected codon sites predicted by Bayes Empirical Bayes method (Yang et al., 2005). 2 Amino acid substuons of the posively selected sites (ancestral states → derived states). 3 Posterior probabilies that these candidate sites have undergone posive selecon. 4 Secondary structures of the loci where posively selected sites are located were predicted by the SOSUI program (hp://bp.nuap.nagoya-u.ac.jp/sosui/). 5 Different branches are shown in different colors. Supplementary Table S2. Candidates for positively selected sites and their amino acid substitution pattern in the terminal branches Gene Site1 Substuon 2 PP3 Secondary Structure4 Branch5 ATP6 119 Arg --> Gln 0.900 Transmembrane Gymnocypris dobula ATP8 37 Pro --> Leu 0.555 Loop region Aspiorhynchus laceps 173 Pro --> Asn 0.819 Loop region Schizothorax plagiostomus 266 Glu --> Trp 0.838 Loop region Schizothorax plagiostomus 307 Ser --> Phe 0.803 Transmembrane Schizothorax richardsonii 353 Leu --> Met 0.575 Transmembrane Schizothorax richardsonii 359 Ser --> Phe 0.803 Transmembrane Schizothorax richardsonii cox1 423 Leu --> Phe 0.804 Transmembrane Schizothorax richardsonii 441 Ser --> Phe 0.803 Loop region Schizothorax richardsonii 461 Ser --> Phe 0.803 Transmembrane Schizothorax richardsonii 465 Val --> Gly 0.820 Transmembrane Schizothorax richardsonii 487 Leu --> Met 0.799 Loop region Schizothorax richardsonii cox2 57 Asp --> Asn 0.829 Loop region Schizothorax labiatus 73 Phe --> Leu 0.808 Loop region Schizothorax richardsonii cox3 178 Ala --> Asn 0.811 Transmembrane Schizothorax plagiostomus cytb 83 His --> Thr 0.962 Transmembrane Aspiorhynchus laceps 25 Pro --> Leu 0.506 Transmembrane Schizothorax richardsonii NADH1 73 Ser --> Phe 0.829 Transmembrane Schizothorax labiatus 192 Ile --> Met 0.819 Transmembrane Schizothorax labiatus NADH2 198 Pro --> Ser 0.898 Transmembrane Gymnocypris dobula NADH3 33 Glu --> Lys 0.835 Loop region Schizothorax labiatus NADH4 235 Ala --> Thr 0.838 Transmembrane Schizothorax labiatus NADH4L 2 Thr --> Ser 0.900 Loop region Gymnocypris dobula 201 Gln --> Ser 0.991 Transmembrane Schizothorax labiatus 253 Ser --> Gly 0.828 Transmembrane Schizothorax labiatus NADH5 266 Leu --> Phe 0.829 Transmembrane Schizothorax labiatus 554 Thr --> Ala 0.643 Loop region Schizothorax richardsonii 1 Posively selected codon sites predicted by Bayes Empirical Bayes method (Yang et al., 2005). 2 Amino acid substuons at posively selected sites (ancestral states → derived states). 3 Posterior probabilies that these candidate sites have undergone posive selecon. 4 Secondary structures of the regions where posively
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