Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Mitogenomic Perspectives on the Adaptation to Extreme Alkaline Environment of Amur ide (Leuciscus waleckii)

Abstract

Amur ide (Leuciscus waleckii, Family Cyprinidae) is widely distributed in Northeast Asia. L. waleckii usually inhabits freshwater environments but can also survive in the Lake Dali Nur, one of the most extreme aquatic environments on the earth, with an alkalinity up to 50 mmol/L (pH 9.6). To investigate mechanisms of mitogenomic evolution underlying adaptation to extreme environments, we determined 30 complete mitogenomes that included Lake Dali Nur (alkaline environment, AL) population and Amur basin (freshwater environment, FW) population. Through phylogenetic and divergence time analysis, we found that AL and FW populations forming distinct two groups which were consistent with geographic divergence (the formation of Lake Dali Nur). In addition, we found that almost of the windows exhibited higher nucleotide diversity in FW population (avg 0.0046) than AL population (avg 0.0012). This result indicated that severe environment selection had remarkably reduced the genetic diversity of mitogenome in AL population and suggested that severe environment selection had remarkably reduced the genetic diversity of mitogenome in the AL population. Compared with the FW population (ω = 0.064), the AL population (ω = 0.092) had a larger mean ω (dN/dS ratios) value for the 13 concatenated mitochondrial protein-coding genes, indicating that the high alkaline tolerated group had accumulated more nonsynonymous mutations. These nonsynonymous mutations had resulted in slightly beneficial amino acid changes that allowed adaption to the severe conditions. This study provides an additional view to decipher the adaptive mitogenome evolution of L. waleckii of the high alkaline environment.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Bureau Du Colombier S, Bolliet Vlambert P, Bardonnet A (2007) Energy and migratory behavior in glass eels (Anguilla anguilla). Physiol Behav 92:684–690

  2. Chang Y, Tang R, Sun X, Liang L, Chen J, Huang J, Dou X, Tao R (2013) Genetic analysis of population differentiation and adaptation in Leuciscus waleckii. Genetica 141:417–429

  3. Chen B, Xu J, Cui J, Pu F, Peng W (2019) Transcriptional differences provide insight into environmental acclimatization in wild Amur ide (Leuciscus waleckii) during spawning migration from alkalized lake to freshwater river. Genomics 111:267–276

  4. Chi B, Chang Y, Yan X, Cao D, Yong L, Gao Y, Liu Y, Liang L (2010) Genetic variability and genetic structure of Leuciscus waleckii Dybowski in Wusuli River and Dali Lake. J Fish Sci China 17:230–235

  5. Collin H, Fumagalli L (2011) Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae). Mol Ecol 20:4490–4502

  6. Cui J, Xu J, Zhang S, Wang K, Jiang Y, Mahboob S, Al-Ghanim KA, Xu P (2015) Transcriptional profiling reveals differential gene expression of Amur ide (Leuciscus waleckii) during spawning migration. Int J Mol Sci 16:13959–13972

  7. Dan M, Eduardo RP, Pawel G, Vincent M, Clark AG, Seyed H, Martin B, Kirk E, Estella C, Brown MD (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci U S A 100:171–176

  8. Dong C, Xu J, Wang B, Feng J, Jeney Z, Sun X, Xu P (2015) Phylogeny and evolution of multiple common carp (Cyprinus carpio L.) populations clarified by phylogenetic analysis based on complete mitochondrial genomes. Mar Biotechnol 17:565

  9. Fabre PH, Rodrigues A, Douzery EJ (2009) Patterns of macroevolution among Primates inferred from a supermatrix of mitochondrial and nuclear DNA. Mol Phylogenet Evol 53:808–825

  10. Feutry P, Castelin M, Ovenden JR, Dettaï A, Robinet T, Cruaud C, Keith P (2013) Evolution of diadromy in fish: insights from a tropical genus (Kuhlia species). Am Nat 181:52–63

  11. Geng K, Zhang Z (1988) The geomorphic characteristics and evolution of the lakes in Dalairuoer area of Neimenggu Plateau during the Holocene. J Beijing Normal Univ 4:94–101

  12. Gienapp P, Teplitsky C, Alho JS, Mills JA, Meril J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

  13. Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Jaffe DB (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A 108:1513–1518

  14. Gu ML, Wang YJ, Shi L, Zhang YB, Chu JY (2009) Comparison on mitochondrial ATP6, ATP8 and Cyt b genes between Chinese Tibetans in three different zones: detecting the signature of natural selection on mitochondrial genome. Hereditas 31:147–152

  15. Gu M, Dong X, Shi L, Shi L, Lin K, Huang X, Chu J (2012) Differences in mtDNA whole sequence between Tibetan and Han populations suggesting adaptive selection to high altitude. Gene 496:0–44

  16. Hélène C, Luca F (2011) Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae). Mol Ecol 20:4490–4502

  17. Hwang PP, Lee TH (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A Mol Integr Physiol 148:479–497

  18. Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, Sado T, Mabuchi K, Takeshima H, Miya M (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol Evol 30:2531–2540

  19. Kamberov YG, Sijia W, Jingze T, Pascale G, Abigail W, Longzhi T, Yajun Y, Shilin L, Kun T, Hua C (2013) Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152:691–702

  20. Kilian B, Ozkan H, Walther A, Kohl J, Dagan T, Salamini F, Martin W (2007) Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (einkorn) domestication: implications for the origin of agriculture. Mol Biol Evol 24:2657–2668

  21. Koch F, Wieser W (1983) Partitioning of energy in fish: can reduction of swimming activity compensate for the cost of production? Nature 116:136–138

  22. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870

  23. Li H, Durbin RJB (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754

  24. Li Y, Ren Z, Shedlock AM, Wu J, Sang L, Tersing T, Hasegawa M, Yonezawa T, Zhong Y (2013) High altitude adaptation of the schizothoracine fishes (Cyprinidae) revealed by the mitochondrial genome analyses. Gene 517:169–178

  25. Li M, Jin L, Ma J, Tian S, Li R, Li X (2016) Detecting mitochondrial signatures of selection in wild Tibetan pigs and domesticated pigs. Mitochondrial DNA 27:747

  26. Linnen CR, Yu Ping P, Peterson BK, Barrett RDH, Larson JG, Jensen JD, Hoekstra HE (2013) Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339:1312–1316

  27. Luo Y (2013) Mitochondrial DNA response to high altitude: a new perspective on high-altitude adaptation. Mitochondrial DNA 24:313–319

  28. Ma B, Lui T, Zhang Y, Chen J (2012) Phylogeography and population genetic structure of Amur Grayling Thymallus grubii in the Amur Basin. Asian Australas J Anim Sci 25:935–944

  29. Mishmar D, Ruizpesini E, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, Easley K, Chen E, Brown MD (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci U S A 100:171–176

  30. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 76:5269–5273

  31. Nosil P (2008) Speciation with gene flow could be common. Mol Biol 17:2103–2106

  32. Permana Maksum I, Saputra SR, Indrayati N, Yusuf M, Subroto T (2017) Bioinformatics study of m.9053G>a mutation at theATP6Gene in relation to type 2 diabetes mellitus and cataract diseases. Bioinf Biol Insights 11:117793221772851

  33. Ren J, Hou Z, Wang H, Sun M-A, Liu X, Liu B, Guo X (2016) Intraspecific variation in mitogenomes of five Crassostrea species provides insight into oyster diversification and speciation. Mar Biotechnol 18:242–254

  34. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

  35. Rundle HD, Nosil P (2010) Ecological speciation. Ecol Lett 8:336–352

  36. Sergey K, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304

  37. Shen YY, Shi P, Sun YB, Zhang YP (2010) Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proc Natl Acad Sci U S A 107:8666–8671

  38. Sudhir K, Glen S, Koichiro T (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

  39. Suk HY, Neff BD (2009) Microsatellite genetic differentiation among populations of the Trinidadian guppy. Heredity 102:425–434

  40. Sun YB, Shen YY, Irwin DM, Zhang YP (2010) Evaluating the roles of energetic functional constraints on teleost mitochondrial-encoded protein, evolution. Mol Biol Evol 28(1):39–44

  41. Sun Y, Shen Y, David MI, Zhang Y (2011) Evaluating the roles of energetic functional constraints on teleost mitochondrial-encoded protein evolution. Mol Biol Evol 28:39

  42. Thomas RH (2000) Molecular evolution and phylogenetics. Heredity 86:385–385

  43. Tomy S, Chang Y, Yh CJ, Wang T, Chang C (2009) Salinity effects on the expression of osmoregulatory genes in the euryhaline black porgy Acanthopagrus schlegeli. Gen Comp Endocrinol 161:123–132

  44. Tong J, Wu Q (2001) Sequence conservation on segments of mitochondrial 16S rRNA and cytochrome B in strains of common carp (Cyprinus Caprio L.Var.). Acta Hydrobiol Sin 25:54–60

  45. Wang Z, Yonezawa T, Liu B, Ma T, Shen X, Su J, Guo S, Hasegawa M, Liu J (2011) Domestication relaxed selective constraints on the yak mitochondrial genome. Mol Biol Evol 28:1553–1556

  46. Wang BS, Ji PF, Xu J, Sun JS, Yang JH, Xu P, Sun XW (2013) Complete mitochondrial genome of Leuciscus waleckii (Cypriniformes: Cyprinidae: Leuciscus). Mitochondrial DNA 24:126–128

  47. Wang Y, Shen Y, Feng C, Zhao K, Song Z, Zhang Y, Yang L, He S (2016) Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Sci Rep 6:29690

  48. Wu XY, Luo J, Huang S, Chen ZM, Xiao H, Zhang YP (2013) Molecular phylogeography and evolutionary history of Poropuntius huangchuchieni (Cyprinidae) in Southwest China. PLoS One 8:e79975

  49. Xiao J, Si B, Zhai D, Itoh S, Lomtatidze Z (2008) Hydrology of Dali Lake in Central-Eastern Inner Mongolia and Holocene East Asian monsoon variability. J Paleolimnol 40:519–528

  50. Xu J, Li Q, Xu L, Wang S, Jiang Y, Zhao Z, Zhang Y, Li J, Dong C, Xu P (2013) Gene expression changes leading extreme alkaline tolerance in Amur ide ( Leuciscus waleckii) inhabiting soda lake. BMC Genomics 14:682

  51. Xu J, Li JT, Jiang Y, Peng W, Yao Z, Chen B, Jiang L, Feng J, Ji P, Liu G (2017) Genomic basis of adaptive evolution: the survival of Amur ide (Leuciscus waleckii) in an extremely alkaline environment. Mol Biol Evol 34:145

  52. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

  53. Yu N, Jensenseaman MI, Chemnick L, Ryder O, Li WH (2004) Nucleotide diversity in gorillas. Genetics 166:1375

  54. Zhao Y, Peng W, Guo H, Chen B, Zhou Z, Xu J, Zhang D, Xu P (2018) Population genomics reveals genetic divergence and adaptive differentiation of Chinese Sea Bass (Lateolabrax maculatus). Mar Biotechnol 20:45–49

  55. Zheng Y, Rui P, Masaki KO, Xiaomao Z (2011) Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of salamanders (order Caudata). Mol Biol Evol 28:2521–2535

  56. Zhou T, Shen X, Irwin DM, Shen Y, Zhang Y (2014) Mitogenomic analyses propose positive selection in mitochondrial genes for high-altitude adaptation in galliform birds. Mitochondrion 18:70–75

Download references

Funding

This study received grant support from the National Natural Science Foundation of China (31801032), the Science and Technology Key Project of Henan Colleges and Universities (17B240001), Science and technology research of Henan province (182102210081), and by the Ph.D. Foundation of Henan Normal University (qd16159).

Author information

PX and XL conceived the study. CD, MY, and XD wrote the manuscript. CD, JZ, and BC performed the bioinformatics analysis to obtain the complete mitochondrial genome sequences. XD, XM, and MZ collected samples. All authors have read and approved the final version of the manuscript.

Correspondence to Xuejun Li or Peng Xu.

Ethics declarations

Competing Interests

The authors declare that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Supplementary Fig. 1
figure6

Neighbor-joining-based phylogenetic tree of CMG sequences in 30 individuals. Bootstrap support value for each branch is included in the tree (PNG 65 kb)

Supplementary Fig. 2
figure7

Bayesian inference-based phylogenetic tree of CMG sequences in 30 individuals. Bayesian posterior probability value for each branch is included in the tree (PNG 425 kb)

High Resolution Image (TIF 668 kb)

High Resolution Image (TIF 676 kb)

ESM 1

The nucleotide variation values of the mitogenome sequences alignments between AL and FW populations using the sliding window approach. (XLS 98 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dong, C., Duan, X., Younis, L.M. et al. Mitogenomic Perspectives on the Adaptation to Extreme Alkaline Environment of Amur ide (Leuciscus waleckii). Mar Biotechnol (2020). https://doi.org/10.1007/s10126-020-09946-7

Download citation

Keywords

  • Leuciscus waleckii
  • Mitogenome
  • Adaptation
  • Alkaline environment