Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 10, 2015

Synonymous and nonsynonymous distances help untangle convergent evolution and recombination

  • Peter B. Chi , Sujay Chattopadhyay , Philippe Lemey , Evgeni V. Sokurenko and Vladimir N. Minin EMAIL logo

Abstract

When estimating a phylogeny from a multiple sequence alignment, researchers often assume the absence of recombination. However, if recombination is present, then tree estimation and all downstream analyses will be impacted, because different segments of the sequence alignment support different phylogenies. Similarly, convergent selective pressures at the molecular level can also lead to phylogenetic tree incongruence across the sequence alignment. Current methods for detection of phylogenetic incongruence are not equipped to distinguish between these two different mechanisms and assume that the incongruence is a result of recombination or other horizontal transfer of genetic information. We propose a new recombination detection method that can make this distinction, based on synonymous codon substitution distances. Although some power is lost by discarding the information contained in the nonsynonymous substitutions, our new method has lower false positive probabilities than the comparable recombination detection method when the phylogenetic incongruence signal is due to convergent evolution. We apply our method to three empirical examples, where we analyze: (1) sequences from a transmission network of the human immunodeficiency virus, (2) tlpB gene sequences from a geographically diverse set of 38 Helicobacter pylori strains, and (3) hepatitis C virus sequences sampled longitudinally from one patient.


Corresponding author: Vladimir N. Minin, Departments of Statistics and Biology, University of Washington, Seattle, WA, 98195, USA, e-mail:

Acknowledgments

We thank Adam Leaché and Ken Rice for helpful comments and discussions. VNM was supported by the National Science Foundation grant DMS-0856099 and the National Institutes of Health grants R01-AI107034 and U54-GM111274. VNM and EVS were supported by the NIH ARRA award 1RC4AI092828. PL acknowledges funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013) under ERC Grant agreement no. 260864.

References

Anisimova, M., R. Nielsen and Z. Yang (2003): “Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites,” Genetics, 164, 1229–1236.10.1093/genetics/164.3.1229Search in Google Scholar PubMed PubMed Central

Arenas, M. and D. Posada (2010a): “Coalescent simulation of intracodon recombination,” Genetics, 184, 429–437.10.1534/genetics.109.109736Search in Google Scholar PubMed PubMed Central

Arenas, M. and D. Posada (2010b): “The effect of recombination on the reconstruction of ancestral sequences,” Genetics, 184, 1133–1139.10.1534/genetics.109.113423Search in Google Scholar PubMed PubMed Central

Awadalla, P. (2003): “The evolutionary genomics of pathogen recombination,” Nat. Rev., 4, 50–60.Search in Google Scholar

Bruen, T. C., H. Philippe and D. Bryant (2006): “A simple robust statistical test for detecting the presence of recombination,” Genetics, 172, 2665–2681.10.1534/genetics.105.048975Search in Google Scholar PubMed PubMed Central

Christin, P. A., G. Besnard, E. J. Edwards and N. Salamin (2012): “Effect of genetic convergence on phylogenetic inference,” Mol. Phylogenet. Evol., 62, 921–927.Search in Google Scholar

Coffin, J. M., S. H. Hughes and H. E. Vamus (1997): Retroviruses, Cold Spring Harbor Laboratory Press.Search in Google Scholar

Croxen, M. A., G. Sisson, R. Melano and P. S. Hoffman (2006): “The Helicobacter pylori chemotaxis receptor tlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa,” J. Bacteriol., 188, 2656–2665.10.1128/JB.188.7.2656-2665.2006Search in Google Scholar PubMed PubMed Central

Feldman, R. A. (2001): Epidemiologic observations and open questions about disease and infection caused by Helicobacter pylori, Horizon Scientific Press.Search in Google Scholar

Feldman, R. A., A. J. P. Eccersley and J. M. Hardie (1998): “Epidemiology of Helicobacter pylori: acquisition, transmission, population prevalence and disease-to-infection ratio,” Br. Med. Bull., 54, 39–53.Search in Google Scholar

Felsenstein, J. F. (2004): Inferring phylogenies, Sinauer Associates.Search in Google Scholar

Goers Sweeney, E., J. N. Henderson, J. Goers, C. Wreden, K. G. Hicks, J. K. Foster, R. Parthasarathy, S. J. Remington and K. Guillemin (2012): “Structure and proposed mechanism for the pH-sensing Helicobacter pylori chemoreceptor tlpB,” Structure, 20, 1177–1188.10.1016/j.str.2012.04.021Search in Google Scholar PubMed PubMed Central

Gonzales, M. J., J. M. Dugan and R. W. Shafer (2002): “Synonymous-non-synonymous mutation rates between sequences containing ambiguous nucleotides (Syn-SCAN),” Bioinformatics, 18, 886–887.10.1093/bioinformatics/18.6.886Search in Google Scholar PubMed PubMed Central

González-Candelas, F., F. X. López-Labrador and M. A. Bracho (2011): “Recombination in hepatitis C virus,” Viruses, 3, 2006–2024.10.3390/v3102006Search in Google Scholar PubMed PubMed Central

Graham, D. Y. (2009): “Efficient identification and evaluation of effective Helicobacter pylori therapies,” Clin. Gasteroenterol. Hepatol., 7, 145–148.Search in Google Scholar

Grassly, N. C. and E. C. Holmes (1997): “A likelihood method for the detection of selection and recombination using nucleotide sequences,” Mol. Biol. Evol., 14, 239–247.Search in Google Scholar

Gray, R. R., M. Salemi, P. Klenerman and O. G. Pybus (2012): “A new evolutionary model for Hepatitis C virus chronic infection,” PLoS Pathog., 8, e1002656.Search in Google Scholar

Hill, M., G. Tachedjian and J. Mak (2005): “The packaging and maturation of the HIV-1 Pol proteins,” Curr. HIV Res., 3, 73–85.Search in Google Scholar

Husmeier, D. and F. Wright (2003): “Detecting recombination in 4-taxa DNA sequence alignments with Bayesian hidden Markov models and Markov chain Monte Carlo,” Mol. Biol. Evol., 20, 315–337.Search in Google Scholar

Irvahn, J., S. Chattopadhyay, E. V. Sokurenko and V. N. Minin (2013): “rbrothers: R package for Bayesian multiple change-point recombination detection,” Evol. Bioinform., 9, 235–238.Search in Google Scholar

Johnson, V. A., F. Brun-Vezinet, B. Clotet, B. Conway, R. T. D’Aquila, L. M. Demeter, D. R. Kuritzkes, D. Pillay, J. M. Schapiro, A. Telenti and D. D. Richman (2003): “Drug resistance mutations in HIV-1,” Top. HIV Med., 11, 215–221.Search in Google Scholar

Lemey, P., I. Derdelinckx, A. Rambaut, K. Van Laethem, S. Dumont, S. Vermeulen and E. Van Wijngaerden (2005): “Molecular footprint of drug-selective pressure in a human immunodeficiency virus transmission chain,” J. Virol., 79, 11981–11989.Search in Google Scholar

Martin, D. P., P. Lemey and D. Posada (2011): “Analysing recombination in nucleotide sequences,” Mol. Ecol. Resources, 11, 943–955.Search in Google Scholar

McGuire, G. and F. Wright (2000): “TOPAL 2.0: improved detection of mosaic sequences within muliple alignments,” Bioinformatics, 16, 130–134.Search in Google Scholar

McGuire, G., F. Wright and M. J. Prentice (1997): “A graphical method for detecting recombination in phylogenetic data sets,” Mol. Biol. Evol., 14, 1125–1131.Search in Google Scholar

Milne, I., F. Wright, G. Rowe, D. F. Marshall, D. Husmeier and G. McGuire (2004): “TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments,” Bioinformatics, 20, 1806–1807.10.1093/bioinformatics/bth155Search in Google Scholar PubMed

Minin, V. N., K. S. Dorman, F. Fang and M. A. Suchard (2005): “Dual multiple change-point model leads to more accurate recombination detection,” Bioinformatics, 21, 3034–3042.10.1093/bioinformatics/bti459Search in Google Scholar PubMed

Morel, V., C. Fournier, C. François, E. Brochot, F. Helle, G. Duverlie and S. Castelain (2011): “Genetic recombination of the hepatitis C virus: clinical implications,” J. Viral Hepat., 18, 77–83.Search in Google Scholar

Nielsen, R. and Z. Yang (1998): “Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene,” Genetics, 148, 929–936.10.1093/genetics/148.3.929Search in Google Scholar

O’Brien, J. D., V. N. Minin and M. A. Suchard (2009): “Learning to count: robust estimates for labeled distances between molecular sequences,” Mol. Biol. Evol., 26, 801–814.Search in Google Scholar

Okamoto, H., K. Kurai, S. I. Okada, K. Yamamoto, H. Iizuka, T. Tanaka, S. Fukuda and F. Tsuda (1992): “Full length sequence of hepatitis C virus genome having poor homology to reported isolates: comparative study of four distinct genotypes,”J. Gen. Virol., 188, 331–341.10.1016/0042-6822(92)90762-ESearch in Google Scholar

Palmer, B. A., I. Moreau, J. Levis, C. Harty, O. Crosbie, E. Kenny-Walsh and L. J. Fanning (2012): “Insertion and recombination events at hypervariable region 1 over 9.6 years of hepatitis c virus chronic infection,” J. Gen. Virol., 93, 2614–2624.Search in Google Scholar

Parsonnet, J., H. Shmuely and T. Haggerty (1999): “Fecal and oral shedding of Helicobacter pylori from healthy infected adults,” J. Am. Med. Assoc., 282, 2240–2245.Search in Google Scholar

Posada, D. and K. A. Crandall (2001): “Evaluation of methods for detecting recombination from DNA sequences: computer simulations,” Proc. Natl. Acad. Sci., 98, 13757–13762.Search in Google Scholar

Posada, D. and K. A. Crandall (2002): “The effect of recombination on the accuracy of phylogenetic estimation,” J. Mol. Evol., 54, 396–402.Search in Google Scholar

Prescott, L. E., A. Berger, J. M. Pawlotsky, P. Conjeevaram, I. Pike and P. Simmonds (1997): “Sequence analysis of hepatitis C virus variants producing discrepant results with two different genotyping assays,” J. Med. Virol., 53, 237–244.Search in Google Scholar

Rambaut, A., D. Posada, K. A. Crandall and E. C. Holmes (2004): “The causes and consequences of HIV evolution,” Nat. Rev. Genet., 5, 52–61.Search in Google Scholar

Schierup, M. H. and J. Hein (2000): “Consequences of recombination on traditional phylogenetic analysis,” Genetics, 156, 879–891.10.1093/genetics/156.2.879Search in Google Scholar PubMed PubMed Central

Smith, D. B., S. Pathirana, F. Davidson, E. Lawlor, J Power, P. L. Yap and P. Simmonds (1997): “The origin of hepatitis C virus genotypes,” J. Gen. Virol., 78, 321–328.Search in Google Scholar

Suchard, M. A., R. E. Weiss, K. S. Dorman and J. S. Sinsheimer (2003): “Inferring spatial phylogenetic variation along nucleotide sequences: a multiple changepoint model,” J. Am. Stat. Assoc., 98, 427–437.Search in Google Scholar

Tenaillon, O., A. Rodriguez-Verdugo, R. L. Gaut, P. McDonald, A. F. Bennett, A. D. Long and B. S. Gaut (2012): “The molecular diversity of adaptive convergence,” Science, 335, 457–461.10.1126/science.1212986Search in Google Scholar PubMed

Tscherne, D. M., M. J. Evans, T. von Hahn, C. T. Jones, Z. Stamataki, J. A. McKeating, B. D. Lindenbach and C. M. Rice (2007): “Superinfection exclusion in cells infected with hepatitis C virus,” J. Virol., 81, 3693–3703.Search in Google Scholar

Viazov, S., A. Widell and E. Nordenfelt (2000): “Mixed infection with two types of hepatitis C virus is probably a rare event,” Infection, 28, 21–25.10.1007/s150100050005Search in Google Scholar PubMed

von Hahn, T., J. C. Yoon, H. Alter, C. M. Rice, B. Rehermann, P. Balfe and J. A. McKeating (2007): “Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo,” Gasterenterology, 132, 667–678.10.1053/j.gastro.2006.12.008Search in Google Scholar PubMed

Wake, D. B., M. H. Wake and C. D. Specht (2011): “Homoplasy: from detecting pattern to determining process and mechanism of evolution,” Science, 331, 1032–1035.10.1126/science.1188545Search in Google Scholar PubMed

WHO (2003): WHO HCV: surveillance and control. http://www.who.int/csr/disease/hepatitis/whocdscsrlyo2003/en/index4.html, 2003. Accessed: 2014-08-11.Search in Google Scholar

Yang, Z. (2006): Computational molecular evolution, Oxford University Press.10.1093/acprof:oso/9780198567028.001.0001Search in Google Scholar

Yang, Z. (2007): “PAML 4: phylogenetic analysis by maximum likelihood,” Mol. Biol. Evol., 24, 1586–1591.Search in Google Scholar

Zibert, Z., E. Schreier and M. Roggendorf (1995): “Antibodies in human sera specific to hypervariable region 1 of hepatitis C virus can block viral attachment,” Virology, 208, 653–661.10.1006/viro.1995.1196Search in Google Scholar PubMed


Supplemental Material:

The online version of this article (DOI: 10.1515/sagmb-2014-0078) offers supplementary material, available to authorized users.


Published Online: 2015-6-10
Published in Print: 2015-8-1

©2015 by De Gruyter

Downloaded on 21.2.2024 from https://www.degruyter.com/document/doi/10.1515/sagmb-2014-0078/html
Scroll to top button