Abstract
We report a strong pattern of molecular-level convergent/parallel evolution of the MYBPC2 gene. Three high-elevation amphibian species, Bufo gargarizans minshanicus, Nanorana pleskei, Rana kukunoris, revealed remarkable numbers of convergent and parallel amino acid substitutions. On the MYBPC2 gene tree of eleven anurans, the three distantly related species formed a strongly supported clade that was away from their respective relatives. Furthermore, we generated both model-based and empirical data-based null distributions for neutral convergent evolution. All three pairwise comparisons among the three species showed significantly more convergent and parallel substitutions than the null distributions. This study adds to the very small roster of clear cases of non-neutral molecular convergent evolution (e.g. prestin, rhodopsin). Molecular convergent evolution has significant implications in biology and detailed case studies will likely provide more insight into its genetic mechanisms.
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References
Castoe TA, de Koning AP, Kim HM, Gu W, Noonan BP, Naylor G, Jiang ZJ, Parkinsons CL, Pollock DD (2009) Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci USA 106:8986–8991
Duellman WE, Trueb L (1994) Biology of amphibians. Johns Hopkins University Press, Baltimore
Fei L, Hu S, Ye C, Huang Y (2009) Fauna China, Amphibia. Science Press, Beijing
Flashman E (2004) Cardiac myosin binding protein c: its role in physiology and disease. Cir Res 94:1279–1289
Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. doi:10.1093/molbev/msw054
Li Y, Liu Z, Shi P, Zhang J (2010) The hearing gene prestin unites echolocating bats and whales. Curr Biol 20:R55–R56
Liu Z, Qi F-Y, Zhou X, Ren H-Q, Shi P (2014) Parallel sites implicate functional convergence of the hearing gene prestin among echolocating mammals. Mol Biol Evol 31:2415–2424
Looso M, Preussner J, Sousounis K, Bruckskotten M, Michel CS, Lignelli E, Reinhardt R, Höffner S, Krüger M, Tsonis PA, Borchardt T, Braun T (2013) A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration. Genome Biol 14:1–16
Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P, Stupka E, Rossiter SJ (2013) Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502:228–231
Pyron R, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61:543–583
Rokas A, Carroll SB (2008) Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol 25:1943–1953
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna 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
Shaffer JF, Gillis TE (2010) Evolution of the regulatory control of vertebrate striated muscle: the roles of troponin I and myosin binding protein-C. Physiol Genom 42:406–419
Shen Y, Liu J, Irwin DM, Zhang YP (2010) Parallel and convergent evolution of the dim-light vision gene RH1 in bats (Order: Chiroptera). PLoS One 5:e8838
Shen Y, Liang L, Li G, Murphy RW, Zhang YP (2012) Parallel evolution of auditory genes for echolocation in bats and toothed whales. PLoS Genet 8:e1002788
Stern DL (2013) The genetic causes of convergent evolution. Nat Rev Genet 14:751–764
Sun YB, Xiong ZJ, Xiang XY, Liu SP, Zhou WW, Tu XL, Zhong L, Wang L, Wu DD, Zhang BL, Zhu CL, Yang MM, Chen HM, Li F, Zhou L, Feng SH, Huang C, Zhang GJ, Irwin D, Hillis DM, Murphy RW, Yang HM, Che J, Wang J, Zhang YP (2015) Whole-genome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes. Proc Natl Acad Sci USA 112:E1257–E1262
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Thomas GW, Hahn MW (2015) Determining the null model for detecting adaptive convergence from genomic data: a case study using echolocating mammals. Mol Biol Evol 32:1232–1236
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Zhang J, Kumar S (1997) Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 14:527–536
Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479
Zou Z, Zhang J (2015a) No genome-wide protein sequence convergence for echolocation. Mol Biol Evol 32:1237–1241
Zou Z, Zhang J (2015b) Are convergent and parallel amino acid substitutions in protein evolution more prevalent than neutral expectations? Mol Biol Evol 32:2085–2096
Acknowledgements
All sequences are deposited at GenBank (accession numbers KY178287-KY178297). This work was supported by the National Nature Science Foundation of China (Grant Number 31328021 to J.F.) and NSERC of Canada (a discovery Grant to J.F.).
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Yang, W., Lu, B. & Fu, J. Molecular Convergent Evolution of the MYBPC2 Gene Among Three High-Elevation Amphibian Species. J Mol Evol 84, 139–143 (2017). https://doi.org/10.1007/s00239-017-9782-z
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DOI: https://doi.org/10.1007/s00239-017-9782-z