Abstract
Phylogenomics has recently revealed that tunicates represent the sister-group of vertebrates in the newly defined clade Olfactores. However, phylogenomic and comparative genomic studies have also suggested that tunicates are characterized by an elevated rate of molecular evolution and a high degree of genomic divergence. Despite the recurrent interest in the group, the picture of tunicate peculiar evolutionary dynamics is still fragmentary, as it mainly lies in studies focusing on only a few model species. In order to expand the available genomic data for the group, we used the high-throughput 454 technology to sequence the partial transcriptome of a previously unsampled tunicate, Microcosmus squamiger. This allowed us to get further insights into tunicate-accelerated evolution through a comparative analysis based on pertinent phylogenetic markers, i.e., a core of 35 housekeeping genes conserved across bilaterians. Our results showed that tunicates evolved on average about two times faster than the other chordates, yet the degree of this acceleration varied extensively upon genes and upon lineages. Appendicularia and Aplousobranchia were detected as the most divergent groups which were also characterized by highly heterogeneous substitution rates across genes. Finally, an estimation of the d N/d S ratio in three pairs of closely related taxa within Olfactores did not reveal strong differences between the tunicate and vertebrate lineages suggesting that for this set of housekeeping genes, the accelerated evolution of tunicates is plausibly due to an elevated mutation rate rather than to particular selective effects.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29
Blaxter M, Thomas J (2004) A survey of genes expressed in the seasquirt Diplosoma listerianum. Unpublished
Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33:W592–W595
Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85–88
Bourlat SJ, Nielsen C, Economou AD, Telford MJ (2008) Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. Mol Phylogenet Evol 49:23–31
Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469–4474
Cañestro C, Postlethwait JH (2007) Development of a chordate anterior-posterior axis without classical retinoic acid signaling. Dev Biol 305:522–538
Cañestro C, Bassham S, Postlethwait JH (2003) Seeing chordate evolution through the Ciona genome sequence. Genome Biol 4:208
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205
Cone AC, Zeller RW (2005) Using ascidian embryos to study the evolution of developmental gene regulatory networks. Can J Zool 83:75–89
Davidson B (2007) Ciona intestinalis as a model for cardiac development. Semin Cell Dev Biol 18:16–26
Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3:e314
Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
Delsuc F, Tsagkogeorga G, Lartillot N, Philippe H (2008) Additional molecular support for the new chordate phylogeny. Genesis 46:592–604
Donmez N, Bazykin GA, Brudno M, Kondrashov AS (2009) Polymorphism due to multiple amino acid substitutions at a codon site within Ciona savignyi. Genetics 181:685–690
Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H (2004) The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci USA 101:15386–15391
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen 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 452:745–749
Edvardsen RB, Lerat E, Maeland AD, Flat M, Tewari R, Jensen MF, Lehrach H, Reinhardt R, Seo HC, Chourrout D (2004) Hypervariable and highly divergent intron-exon organizations in the chordate Oikopleura dioica. J Mol Evol 59:448–457
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) In: Department of genome sciences UoW (ed), Seattle
Gissi C, Pesole G, Cattaneo E, Tartari M (2006) Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus. BMC Genomics 7:288
Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 101:301–320
Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736
Goldstone JV, Goldstone HM, Morrison AM, Tarrant A, Kern SE, Woodin BR, Stegeman JJ (2007) Cytochrome P450 1 genes in early deuterostomes (tunicates and sea urchins) and vertebrates (chicken and frog): origin and diversification of the CYP1 gene family. Mol Biol Evol 24:2619–2631
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Gyoja F, Satou Y, Shin-i T, Kohara Y, Swalla BJ, Satoh N (2007) Analysis of large scale expression sequenced tags (ESTs) from the anural ascidian, Molgula tectiformis. Dev Biol 307:460–482
Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Muller WE, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 276:4261–4270
Holland LZ, Gibson-Brown JJ (2003) The Ciona intestinalis genome: when the constraints are off. Bioessays 25:529–532
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
Ikuta T, Yoshida N, Satoh N, Saiga H (2004) Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci USA 101:15118–15123
Imai KS, Levine M, Satoh N, Satou Y (2006) Regulatory blueprint for a chordate embryo. Science 312:1183–1187
Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518
Kim YO, Cho HK, Park EM, Nam BH, Hur YB, Lee SJ, Cheong J (2008) Generation of expressed sequence tags for immune gene discovery and marker development in the sea squirt, Halocynthia roretzi. J Microbiol Biotechnol 18:1510–1517
Kim JH, Waterman MS, Li LM (2007) Diploid genome reconstruction of Ciona intestinalis and comparative analysis with Ciona savignyi. Genome Res 17:1101–1110
Kimbacher S, Gerstl I, Velimirov B, Hagemann S (2009) Drosophila P transposons of the urochordata Ciona intestinalis. Mol Genet Genomics 282:165–172
Kowalevski A (1868) Beiträge zur Entwicklungsgeschichte der Tunicaten. Nachrichten Gesellschaft Wissenschaften Göttingen 19:401–415
Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304
Lambert C (2005) Historical introduction, overview, and reproductive biology of the protochordates. Can J Zool 83:1–7
Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21:1095–1109
Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3. A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286–2288
Le SQ, Gascuel O, Lartillot N (2008) Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24:2317–2323
Mallatt J, Winchell CJ (2007) Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star. Mol Phylogenet Evol 43:1005–1022
Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380
Nabholz B, Glemin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Perez-Portela R, Bishop JD, Davis AR, Turon X (2009) Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 50:560–570
Philippe H, Sorhannus U, Baroin A, Perasso R, Gasse F, Adoutte A (1994) Comparison of molecular and paleontological data in diatoms suggests a major gap in the fossil record. J Evol Biol 7:247–265
Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071
Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14
Rius M, Turon X, Marshall DJ (2009) Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages. Oecologia 159:873–882
Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295
Seo HC, Kube M, Edvardsen RB, Jensen MF, Beck A, Spriet E, Gorsky G, Thompson EM, Lehrach H, Reinhardt R, Chourrout D (2001) Miniature genome in the marine chordate Oikopleura dioica. Science 294:2506
Seo HC, Edvardsen RB, Maeland AD, Bjordal M, Jensen MF, Hansen A, Flaat M, Weissenbach J, Lehrach H, Wincker P, Reinhardt R, Chourrout D (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431:67–71
Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145
Sierro N, Kusakabe T, Park KJ, Yamashita R, Kinoshita K, Nakai K (2006) DBTGR: a database of tunicate promoters and their regulatory elements. Nucleic Acids Res 34:D552–D555
Singh TR, Tsagkogeorga G, Delsuc F, Blanquart S, Shenkar N, Loya Y, Douzery EJ, Huchon D (2009) Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny. BMC Genomics 10:534
Small KS, Brudno M, Hill MM, Sidow A (2007a) Extreme genomic variation in a natural population. Proc Natl Acad Sci USA 104:5698–5703
Small KS, Brudno M, Hill MM, Sidow A (2007b) A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol 8:R41
Swalla BJ, Xavier-Neto J (2008) Chordate origins and evolution. Genesis 46:575–579
Swalla BJ, Cameron CB, Corley LS, Garey JR (2000) Urochordates are monophyletic within the deuterostomes. Syst Biol 49:52–64
Swofford D (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates Sunderland, Massachusetts
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Telford MJ (2006) Animal phylogeny. Curr Biol 16:R981–R985
The R Development CoreTeam (2004) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657
Tsagkogeorga G, Turon X, Hopcroft RR, Tilak MK, Feldstein T, Shenkar N, Loya Y, Huchon D, Douzery EJ, Delsuc F (2009) An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol Biol 9:187
Turon X, Lopez-Legentil S (2004) Ascidian molecular phylogeny inferred from mtDNA data with emphasis on the Aplousobranchiata. Mol Phylogenet Evol 33:309–320
Winchell CJ, Sullivan J, Cameron CB, Swalla BJ, Mallatt J (2002) Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol 19:762–776
Wolf JB, Kunstner A, Nam K, Jakobsson M, Ellegren H (2009) Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection. Genome Biol Evol 2009:308–319
Yandell M, Mungall CJ, Smith C, Prochnik S, Kaminker J, Hartzell G, Lewis S, Rubin GM (2006) Large-scale trends in the evolution of gene structures within 11 animal genomes. PLoS Comput Biol 2:e15
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449
Yokobori S, Kurabayashi A, Neilan BA, Maruyama T, Hirose E (2006) Multiple origins of the ascidian-Prochloron symbiosis: molecular phylogeny of photosymbiotic and non-symbiotic colonial ascidians inferred from 18S rDNA sequences. Mol Phylogenet Evol 40:8–19
Zeng L, Swalla B (2005) Molecular phylogeny of the protochordates: chordate evolution. Can J Zool 83:24–33
Zeng L, Jacobs M, Swalla B (2006) Coloniality and sociality has evolved once in Stolidobranch ascidians. Integr Comp Biol 46:255–268
Acknowledgments
We thank the associated editor and two anonymous referees for their constructive comments. This study has been supported by the Research Networks Program in Bioinformatics of the High Council for Scientific and Technological Cooperation between France and Israel, by the European Research Council (‘PopPhyl’: Population Phylogenomics), and benefited from the ISE-M computing cluster. This study is contribution to ISEM 2010-049 of the Institut des Sciences de l’Evolution de Montpellier (UMR 5554-CNRS).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tsagkogeorga, G., Turon, X., Galtier, N. et al. Accelerated Evolutionary Rate of Housekeeping Genes in Tunicates. J Mol Evol 71, 153–167 (2010). https://doi.org/10.1007/s00239-010-9372-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-010-9372-9