Hong JIN,Bin LU and Jinzhong FU.Massive Molecular Parallel Evolution of the HSP90AA1 Gene between High-elevation Anurans[J].Asian Herpetological Research(AHR),2018,9(3):195-200.[doi:10.16373/j.cnki.ahr.180039]
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Massive Molecular Parallel Evolution of the HSP90AA1 Gene between High-elevation Anurans
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2018 VoI.9 No.3
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Massive Molecular Parallel Evolution of the HSP90AA1 Gene between High-elevation Anurans
Hong JIN1 Bin LU1 and Jinzhong FU12*
1 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China
2 Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G2W1, Canada
molecular parallel evolution high-elevation case study amphibian HSP90AA1 gene
HSP90AA1 is part of the heat shock protein 90 gene family and has important functions against heat stress. We report a case of molecular level parallel evolution of the HSP90AA1 gene in high elevation amphibians. HSP90AA1 gene sequences of four high-elevation anurans, Bufo gargarizans, Nanorana parkeri, Rana kukunoris, and Scutiger boulengeri, were compared along with five of their low-elevation relatives. A total of 16 amino-acid sites were identified as parallel evolution between N. parkeri and R. kukunoris. We generated both model based (Zhang and Kumar’s test) and empirical data based (parallel/divergence plotting) null distributions for non-parallel evolution, and both methods clearly determined that the observed number of parallel substitutions were significantly more than the null expectation. Furthermore, on the HSP90AA1 gene tree, N. parkeri and R. kukunoris formed a strongly supported clade that was away from their respective relatives. This study provides a clear case of molecular parallel evolution, which may have significant implications in understanding the genetic mechanisms of high-elevation adaptation.


Castoe T. A., de Koning A. P., Kim H. M., Gu W., Noonan B. P., Naylor G., Jiang Z. J., Parkinsons C. L., Pollock D. D. 2009. Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci USA, 106: 8986–8991
Cheviron Z. A., Brumfield R. T. 2012. Genomic insights into adaptation to high-altitude environments. Heredity, 108: 354–361
Duellman W. E., Trueb L. 1994. Biology of Amphibians. Baltimore, USA: Johns Hopkins University Press
Gerchen J. F., Reichert S. J., R?hr J. T., Dieterich C., Kloas W., St?ck M. 2016. A single transcriptome of a green toad (Bufo viridis) yields candidate genes for sex determination and differentiation and non-anonymous population genetic markers. PLoS ONE, 11: e0156419
Hellsten U., Harland R. M., Gilchrist M. J., and 48 other authors. 2010. The genome of the western clawed frog Xenopus tropicalis. Science, 328: 633–636
Li P., Zhao E., Dong B. 2010. Amphibians and Reptiles of Tibet. Beijing, China: Science Press
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
NCBI. 2018. https://www.ncbi.nlm.nih.gov/gene/3320
Parker J., Tsagkogeorga G., Cotton J. A., Liu Y., Provero P., Stupka E., Rossiter S. J. 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature, 502: 228–231
Pyron R., Wiens J. J. 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
Qiao L., Yang W., Fu J., Song Z. 2013. Transcriptome profile of the green odorous frog (Odorrana margaratea). PLoS ONE, 8: e75211
R Core Team. 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Rokas A., Carroll S. B. 2008. Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol, 25: 1943–1953
Simonson T. S., Yang Y., Huff C. D., Yun H., Qin G., Witherspoon D. J., Bai Z., Lorenzo F. R., Xing J., Jorde L. B. 2010. Genetic evidence for high-altitude adaptation in Tibet. Science, 329: 72–75.
Scott G. R., Schulte P. M., Egginton S., Scott A. L. M., Richards J. G., Milsom W. K. 2011. Molecular evolution of cytochrome c oxidase underlies high-altitude adaptation in the bar-headed goose. Mol Biol Evol, 28: 351–363.
Shen Y., Liu J., Irwin D. M., Zhang Y. P. 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 R. W., Zhang Y. P. 2012. Parallel evolution of auditory genes for echolocation in bats and toothed whales. PLoS Genet, 8: e1002788
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30: 1312–1213.
Stern D. L. 2013. The genetic causes of convergent evolution. Nat Rev Genet, 14: 751–764
Sun Y. B., Xiong Z. J., Xiang X. Y., Liu S. P., Zhou W. W., Tu X. L., Zhong L., Wang L., Wu D. D., Zhang B. L., Zhu C. L., Yang M. M., Chen H. M., Li F., Zhou L., Feng S. H., Huang C., Zhang G. J., Irwin D., Hillis D. M., Murphy R. W., Yang H. M., Che J., Wang J., Zhang Y. P. 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
Thomas G. W, Hahn M. W. 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 W., Qi Y., Bi K., Fu J. 2012. Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species: A comparative transcriptomic analysis of two ranid frogs, Rana chensinensis and R. kukunoris. BMC Genomics, 13: 588
Yang W., Qi Y., Fu J. 2016. Genetic signals of high-altitude adaptation in amphibians: A comparative transcriptome analysis. BMC Genet, 17: 134
Yang W., Lu B., Fu J. 2017. Molecular convergent evolution of the MYBPC2 gene among three high-elevation amphibian species. J Mol Evol, 84: 139–143
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
Zhao E., Yang D. 1997. Amphibians and Reptiles of the Hengduan Mountain region. Beijing, China: Science Press
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


Last Update: 2018-09-26