Skip to main content

Recovering the Tree-Like Trend of Evolution Despite Extensive Lateral Genetic Transfer: A Probabilistic Analysis

  • Conference paper
Research in Computational Molecular Biology (RECOMB 2012)

Part of the book series: Lecture Notes in Computer Science ((LNBI,volume 7262))

Abstract

Lateral gene transfer (LGT) is a common mechanism of non-vertical evolution where genetic material is transferred between two more or less distantly related organisms. It is particularly common in bacteria where it contributes to adaptive evolution with important medical implications. In evolutionary studies, LGT has been shown to create widespread discordance between gene trees as genomes become mosaics of gene histories. In particular, the Tree of Life has been questioned as an appropriate representation of bacterial evolutionary history. Nevertheless a common hypothesis is that prokaryotic evolution is primarily tree-like, but that the underlying trend is obscured by LGT. Extensive empirical work has sought to extract a common tree-like signal from conflicting gene trees. Here we give a probabilistic perspective on the problem of recovering the tree-like trend despite LGT. Under a model of randomly distributed LGT, we show that the species phylogeny can be reconstructed even in the presence of surprisingly many (almost linear number of) LGT events per gene tree. Our results, which are optimal up to logarithmic factors, are based on the analysis of a robust, computationally efficient reconstruction method and provides insight into the design of such methods. Finally we show that our results have implications for the discovery of highways of gene sharing.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arvestad, L., Lagergren, J., Sennblad, B.: The gene evolution model and computing its associated probabilities. J. ACM 56(2) (2009)

    Google Scholar 

  2. Baum, B.R.: Combining trees as a way of combining data sets for phylogenetic inference. Taxon 41, 3–10 (1992)

    Article  Google Scholar 

  3. Bansal, M.S., Banay, G., Peter Gogarten, J., Shamir, R.: Detecting highways of horizontal gene transfer. Journal of Computational Biology 18(9), 1087–1114 (2011)

    Article  MathSciNet  Google Scholar 

  4. Bandelt, H.-J., Dress, A.: Reconstructing the shape of a tree from observed dissimilarity data 7, 309–343 (1986)

    Google Scholar 

  5. Berry, V., Gascuel, O.: Inferring evolutionary trees with strong combinatorial evidence. Theoretical Computer Science (240), 271–298 (2001)

    Google Scholar 

  6. Beiko, R.G., Harlow, T.J., Ragan, M.A.: Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. USA 102, 14332–14337 (2005)

    Article  Google Scholar 

  7. Bapteste, E., Susko, E., Leigh, J., MacLeod, D., Charlebois, R.L., Doolittle, W.F.: Do orthologous gene phylogenies really support tree-thinking? BMC Evol. Biol. 5, 33 (2005)

    Article  Google Scholar 

  8. Buneman, P.: The recovery of trees from measures of dissimilarity. In: Hodson, F.R., Kendall, D.G., Tautu, P. (eds.) Anglo-Romanian Conference on Mathematics in the Archaeological and Historical Sciences, pp. 387–395. Edinburgh University Press, Mamaia (1971)

    Google Scholar 

  9. Chung, Y., Ane, C.: Comparing two bayesian methods for gene tree/species tree reconstruction: Simulations with incomplete lineage sorting and horizontal gene transfer. Systematic Biology 60(3), 261–275 (2011)

    Article  Google Scholar 

  10. Csűrös, M., Miklós, I.: A Probabilistic Model for Gene Content Evolution with Duplication, Loss, and Horizontal Transfer. In: Apostolico, A., Guerra, C., Istrail, S., Pevzner, P.A., Waterman, M. (eds.) RECOMB 2006. LNCS (LNBI), vol. 3909, pp. 206–220. Springer, Heidelberg (2006)

    Chapter  Google Scholar 

  11. Doolittle, W.F., Bapteste, E.: Pattern pluralism and the tree of life hypothesis. Proc. Natl. Acad. Sci. USA 104, 2043–2049 (2007)

    Article  Google Scholar 

  12. Delsuc, F., Brinkmann, H., Philippe, H.: Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 6(5), 361–375 (2005)

    Article  Google Scholar 

  13. Dagan, T., Martin, W.: The tree of one percent. Genome Biology 7(10), 118 (2006)

    Article  Google Scholar 

  14. Daskalakis, C., Mossel, E., Roch, S.: Evolutionary trees and the ising model on the bethe lattice: a proof of steel’s conjecture. Probability Theory and Related Fields 149, 149–189 (2011), doi:10.1007/s00440-009-0246-2

    Article  MathSciNet  MATH  Google Scholar 

  15. Degnan, J.H., Rosenberg, N.A.: Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology and Evolution 24(6), 332–340 (2009)

    Article  Google Scholar 

  16. Daskalakis, C., Roch, S.: Alignment-Free Phylogenetic Reconstruction. In: Berger, B. (ed.) RECOMB 2010. LNCS, vol. 6044, pp. 123–137. Springer, Heidelberg (2010)

    Chapter  Google Scholar 

  17. Dewhirst, F.E., Shen, Z., Scimeca, M.S., Stokes, L.N., Boumenna, T., Chen, T., Paster, B.J., Fox, J.G.: Discordant 16S and 23S rRNA gene phylogenies for the Genus Helicobacter: Implications for phylogenetic inference and systematics. J. Bacteriol. 187(17), 6106–6118 (2005)

    Article  Google Scholar 

  18. Eisen, J.A., Fraser, C.M.: Phylogenomics: Intersection of evolution and genomics. Science 300(5626), 1706–1707 (2003)

    Article  Google Scholar 

  19. Galtier, N.: A model of horizontal gene transfer and the bacterial phylogeny problem. Systematic Biology 56(4), 633–642 (2007)

    Article  Google Scholar 

  20. Galtier, N., Daubin, V.: Dealing with incongruence in phylogenomic analyses. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 4023–4029 (2008)

    Article  Google Scholar 

  21. Peter Gogarten, J., Ford Doolittle, W., Lawrence, J.G.: Prokaryotic evolution in light of gene transfer. Molecular Biology and Evolution 19(12), 2226–2238 (2002)

    Article  Google Scholar 

  22. Peter Gogarten, J., Townsend, J.P.: Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Micro. 3(9), 679–687 (2005)

    Article  Google Scholar 

  23. Ge, F., Wang, L.S., Kim, J.: The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PLoS Biol. 3, e316 (2005)

    Article  Google Scholar 

  24. Huson, D.H., Rupp, R., Scornavacca, C.: Phylogenetic Networks: Concepts, Algorithms and Applications. Cambridge University Press, Cambridge (2010)

    Book  Google Scholar 

  25. Joly, S., McLenachan, P.A., Lockhart, P.J.: A statistical approach for distinguishing hybridization and incomplete lineage sorting. The American Naturalist 174(2), E54–E70 (2009)

    Article  Google Scholar 

  26. Jin, G., Nakhleh, L., Snir, S., Tuller, T.: Maximum likelihood of phylogenetic networks. Bioinformatics 22(21), 2604–2611 (2006)

    Article  Google Scholar 

  27. Jin, G., Nakhleh, L., Snir, S., Tuller, T.: Parsimony score of phylogenetic networks: Hardness results and a linear-time heuristic. IEEE/ACM Trans. Comput. Biology Bioinform. 6(3), 495–505 (2009)

    Article  Google Scholar 

  28. Koonin, E.V.: The biological big bang model for the major transitions in evolution. Biol. Direct. 2, 21 (2007)

    Article  Google Scholar 

  29. Koonin, E.V., Puigbo, P., Wolf, Y.I.: Comparison of phylogenetic trees and search for a central trend in the forest of life. Journal of Computational Biology 18(7), 917–924 (2011)

    Article  MathSciNet  Google Scholar 

  30. Kim, J., Salisbury, B.A.: A tree obscured by vines: Horizontal gene transfer and the median tree method of estimating species phylogeny. In: Pacific Symposium on Biocomputing, pp. 571–582 (2001)

    Google Scholar 

  31. Kubatko, L.S.: Identifying hybridization events in the presence of coalescence via model selection. Systematic Biology 58(5), 478–488 (2009)

    Article  Google Scholar 

  32. Lindvall, T.: Lectures on the Coupling Method. Wiley, New York (1992)

    MATH  Google Scholar 

  33. Maddison, W.P.: Gene trees in species trees. Systematic Biology 46(3), 523–536 (1997)

    Article  Google Scholar 

  34. Meng, C., Kubatko, L.S.: Detecting hybrid speciation in the presence of incomplete lineage sorting using gene tree incongruence: A model. Theoretical Population Biology 75(1), 35–45 (2009)

    Article  MATH  Google Scholar 

  35. Mossel, E.: Phase transitions in phylogeny. Trans. Amer. Math. Soc. 356(6), 2379–2404 (2004)

    Article  MathSciNet  MATH  Google Scholar 

  36. Eisen, J.A., Fraser, C.M.: Phylogenomics: Intersection of evolution and genomics. Science 300(5626), 1706–1707 (2003)

    Article  Google Scholar 

  37. Puigbo, P., Wolf, Y.I., Koonin, E.V.: The tree and net components of prokaryote evolution. Genome Biology and Evolution 2, 745–756 (2010)

    Article  Google Scholar 

  38. Ragan, M.A.: Matrix representation in reconstructing phylogenetic-relationships among the eukaryotes. Biosystems 28, 47–55 (1992)

    Article  Google Scholar 

  39. Ragan, M.A., Beiko, R.G.: Lateral genetic transfer: open issues. Philosophical Transactions of the Royal Society B: Biological Sciences 364(1527), 2241–2251 (2009)

    Article  Google Scholar 

  40. Rannala, B., Yang, Z.: Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. J. Mol. Evol. 43, 304–311 (1996)

    Article  Google Scholar 

  41. Smets, B.F., Barkay, T.: Horizontal gene transfer: perspectives at a crossroads of scientific disciplines. Nat. Rev. Micro. 3(9), 675–678 (2005)

    Article  Google Scholar 

  42. Snir, S., Rao, S.: Quartets maxcut: A divide and conquer quartets algorithm. IEEE/ACM Trans. Comput. Biology Bioinform. 7(4), 704–718 (2010)

    Article  Google Scholar 

  43. Snir, S., Rao, S.: Quartet maxcut: A fast algorithm for amalgamating quartet trees. Molecular Phylogenetics and Evolution 62(1), 1–8 (2012)

    Article  Google Scholar 

  44. Semple, C., Steel, M.: Phylogenetics. Mathematics and its Applications series, vol. 22. Oxford University Press (2003)

    Google Scholar 

  45. Schouls, L.M., Schot, C.S., Jacobs, J.A.: Horizontal transfer of segments of the 16S rRNA genes between species of the Streptococcus anginosus group. J. Bacteriol. 185(24), 7241–7246 (2003)

    Article  Google Scholar 

  46. Steel, M.: The complexity of reconstructing trees from qualitative characters and subtress. Journal of Classification 9(1), 91–116 (1992)

    Article  MathSciNet  MATH  Google Scholar 

  47. Suchard, M.A.: Stochastic models for horizontal gene transfer. Genetics 170(1), 419–431 (2005)

    Article  MathSciNet  Google Scholar 

  48. Than, C., Ruths, D., Innan, H., Nakhleh, L.: Confounding factors in hgt detection: Statistical error, coalescent effects, and multiple solutions. Journal of Computational Biology 14(4), 517–535 (2007)

    Article  MathSciNet  Google Scholar 

  49. van Berkum, P., Terefework, Z., Paulin, L., Suomalainen, S., Lindstrom, K., Eardly, B.D.: Discordant phylogenies within the rrn loci of rhizobia. J. Bacteriol. 185(10), 2988–2998 (2003)

    Article  Google Scholar 

  50. Yu, Y., Than, C., Degnan, J.H., Nakhleh, L.: Coalescent histories on phylogenetic networks and detection of hybridization despite incomplete lineage sorting. Systematic Biology 60(2), 138–149 (2011)

    Article  Google Scholar 

  51. Yap, W.H., Zhang, Z., Wang, Y.: Distinct types of rrna operons exist in the genome of the Actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J. Bacteriol. 181(17), 5201–5209 (1999)

    Google Scholar 

  52. Eisen, J.A., Fraser, C.M.: Phylogenomics: Intersection of evolution and genomics. Science 300(5626), 1706–1707 (2003)

    Article  Google Scholar 

  53. Zhaxybayeva, O., Lapierre, P., Gogarten, J.P.: Genome mosaicism and organismal lineages. Trends Genet 20, 254–260 (2004)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Roch, S., Snir, S. (2012). Recovering the Tree-Like Trend of Evolution Despite Extensive Lateral Genetic Transfer: A Probabilistic Analysis. In: Chor, B. (eds) Research in Computational Molecular Biology. RECOMB 2012. Lecture Notes in Computer Science(), vol 7262. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-29627-7_23

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-29627-7_23

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-29626-0

  • Online ISBN: 978-3-642-29627-7

  • eBook Packages: Computer ScienceComputer Science (R0)

Publish with us

Policies and ethics