Quartet Partitioning Reveals Hybrid Origins of the Vertebrate

  • Michael Syvanen
  • Bryan Ericksen
  • Simone Linz
  • Jonathan Ducore
Chapter

Abstract

It is generally accepted that humans and sea urchins are deuterostomes and that fruit flies and jelly fish are outgroups. However, when we analyzed proteins from the genomes of these four species and submitted them to 4 taxa phylogenetic analysis, we found that, while as expected, most of the proteins (563) supported the notion of human and sea urchin in one clade and jelly fish and fruit flies in the other clade (Tree1), a large number of proteins (353) showed human and fruit fly in one clade with the sea urchin and jelly fish in the other (Tree3). Homologs were found in the genomes from 5 other metazoa. Tree1 proteins resulted in the expected 9 taxa tree, while the Tree3 proteins show vertebrates, to the exclusion of the other chordates, in the protostome clade. The two 9 taxa trees were fused into a single most parsimonious net that supports an introgression event between a vertebrate ancestor and a primitive protostome.

References

  1. Baroni M, Grünewald S, Moulton V, Semple C (2005) Bounding the number of hybridisation events for a consistent evolutionary history. J Math Biol 51:171–182PubMedCrossRefGoogle Scholar
  2. Blair JE, Blair Hedges S (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284PubMedCrossRefGoogle Scholar
  3. Blair JE, Ikeo K, Gojobori T, Hedges SB (2002) The evolutionary position of nematodes. BMC Evol Biol 8(2):7CrossRefGoogle Scholar
  4. C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 11:2012–2018CrossRefGoogle Scholar
  5. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedCrossRefGoogle Scholar
  6. Celniker et al (2002) Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol 3:1–0079CrossRefGoogle Scholar
  7. Collins J, Linz S, Semple C (2011) Quantifying hybridization in realistic time. J Comput Biol 18:1305–1318PubMedCrossRefGoogle Scholar
  8. Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968PubMedCrossRefGoogle Scholar
  9. DeSalle R, Schierwater B (2008) An even newer animal phylogeny. BioEssays 30:1043–1047PubMedCrossRefGoogle Scholar
  10. Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H (2004) The timing of eukaryotic evolution. Proc Natl Acad Sci USA 101:15386–15391Google Scholar
  11. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  12. Eitel M, Osigus HJ, DeSalle R, Schierwater B (2013) Global diversity of the Placozoa. PLoS One 8(4):e57131PubMedCentralPubMedCrossRefGoogle Scholar
  13. Felsenstein J (2005) PHYLIP (Phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  14. Fuchs J, Obst M, Sundberg P (2009) The first comprehensive molecular phylogeny of Bryozoa (Ectoprocta) based on combined analyses of nuclear and mitochondrial genes. Mol Phylogenet Evol 52:225–233Google Scholar
  15. Gaut BS, Lewis PO (1995) Success of maximum likelihood phylogeny inference in the four-taxon case. Mol Biol Evol 12:152–162PubMedCrossRefGoogle Scholar
  16. Gauthier O, Lapointe F (2007) Hybrids and phylogenetics revisited: a statistical test of hybridization using quartets. Syst Bot 32:8–15CrossRefGoogle Scholar
  17. Hillis DM, Huelsenbeck JP (1992) Signal, noise, and reliability in molecular phylogenetic analyses. J Hered 83:189–195Google Scholar
  18. Hughes AL, Friedman R (2003) 2R or not 2R: testing hypotheses of genome duplication in early vertebrates. J Struct Funct Genomics 3:85–93PubMedCrossRefGoogle Scholar
  19. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  20. Huson DH, Scornavacca C (2011) A survey of combinatorial methods for phylogenetic networks. Genome Biol Evol 3:23–35PubMedCentralPubMedCrossRefGoogle Scholar
  21. JGI X. tropicalis genome assembly (2009). http://genome.jgi-psf.org/Xentr4/Xentr4.home.html
  22. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  23. Lecointre G, Philippe H, Vân Lê HL, Le Guyader H (1993) Species sampling has a major impact on phylogenetic inference. Mol Phylogenet Evol 2:205–224PubMedCrossRefGoogle Scholar
  24. Matus DQ, Copley RR, Dunn CW, Hejnol A, Eccleston H, Halanych KM, Martindale MQ, Telford MJ (2006) Broad taxon and gene sampling indicate that chaetognaths are protostomes. Curr Biol 8:R575–R576CrossRefGoogle Scholar
  25. Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Müller WE, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G (2013) Deep metazoan phylogeny: when different genes tell different stories. Phylogenet Evol 67:223–233CrossRefGoogle Scholar
  26. Osigus HJ, Eitel M, Bernt M, Donath A, Schierwater B (2013) Mitogenomics at the base of Metazoa. Mol Phylogenet Evol 69:339–351Google Scholar
  27. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  28. Peterson KJ, Cotton JA, Gehling JG, Pisani D (2008) The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc Lond B Biol Sci 363:1435–1443PubMedCentralPubMedCrossRefGoogle Scholar
  29. Philip GK, Creevey CJ, McInerney JO (2005) The Opisthokonta and the Ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. Mol Biol Evol 22:1175–1184PubMedCrossRefGoogle Scholar
  30. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Wörheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712PubMedCrossRefGoogle Scholar
  31. Putnam NH, T Butts, Ferrier DEK, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguch E, Terry A et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071Google Scholar
  32. Sea Urchin Genome Sequencing Consortium, Sodergren E et al (2006) The Genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952Google Scholar
  33. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116CrossRefGoogle Scholar
  34. Srivastava, M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–960Google Scholar
  35. Sullivan JC, Ryan JF, Watson JA, Webb J, Mullikin JC, Rokhsar D, Finnerty JR (2006) StellaBase: the Nematostella vectensis genomics database. Nucleic Acids Res 1:34Google Scholar
  36. Syvanen M (1985) Cross-species gene transfer: implications for a new theory of evolution. J Theor Biol 112:333–343PubMedCrossRefGoogle Scholar
  37. Syvanen M (2002) On the occurence of horizontal gene transfer among an arbitrarily chosen group of 26 Genes. J Mol Evol 54:258–266PubMedCrossRefGoogle Scholar
  38. Syvanen M (2012) Evolutionary implications of horizontal gene transfer. Ann Rev Genet 46:341–358PubMedCrossRefGoogle Scholar
  39. Syvanen M, Ducore J (2010) Whole genome comparisons reveals a possible chimeric origin for a major metazoan assemblage source. J Biol Syst 18:261–275Google Scholar
  40. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralPubMedCrossRefGoogle Scholar
  41. Wray GA, Levinton JS, Shapiro LH (1996) Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274:568–573CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Michael Syvanen
    • 1
  • Bryan Ericksen
    • 1
  • Simone Linz
    • 2
  • Jonathan Ducore
    • 3
  1. 1.Department of MicrobiologyUniversity of California at Davis School of MedicineDavisUSA
  2. 2.Department of Computer Science, Center for Bioinformatics (ZBIT)University of TübingenTübingenGermany
  3. 3.Department of PediatricsUniversity of California at Davis School of MedicineDavisUSA

Personalised recommendations