Hemichordate genomes and deuterostome origins

Simakov, Oleg; Kawashima, Takeshi; Marlétaz, Ferdinand; Jenkins, Jerry; Koyanagi, Ryo; Mitros, Therese; Hisata, Kanako; Bredeson, Jessen; Shoguchi, Eiichi; Gyoja, Fuki; Yue, Jia-Xing; Chen, Yi-Chih; Freeman, Robert M.; Sasaki, Akane; Hikosaka-Katayama, Tomoe; Sato, Atsuko; Fujie, Manabu; Baughman, Kenneth W.; Levine, Judith; Gonzalez, Paul; Cameron, Christopher; Fritzenwanker, Jens H.; Pani, Ariel M.; Goto, Hiroki; Kanda, Miyuki; Arakaki, Nana; Yamasaki, Shinichi; Qu, Jiaxin; Cree, Andrew; Ding, Yan; Dinh, Huyen H.; Dugan, Shannon; Holder, Michael; Jhangiani, Shalini N.; Kovar, Christie L.; Lee, Sandra L.; Lewis, Lora R.; Morton, Donna; Nazareth, Lynne V.; Okwuonu, Geoffrey; Santibanez, Jireh; Chen, Rui; Richards, Stephen; Muzny, Donna M.; Gillis, Andrew; Peshkin, Leonid; Wu, Michael; Humphreys, Tom; Su, Yi-Hsien; Putnam, Nicholas H.; Schmutz, Jeremy; Fujiyama, Asao; Yu, Jr-Kai; Tagawa, Kunifumi; Worley, Kim C.; Gibbs, Richard A.; Kirschner, Marc W.; Lowe, Christopher J.; Satoh, Noriyuki; Rokhsar, Daniel S.; Gerhart, John

doi:10.1038/nature16150

Hemichordate genomes and deuterostome origins

Journal Article · Sun Nov 01 00:00:00 EDT 2015 · Nature (London)

DOI:https://doi.org/10.1038/nature16150· OSTI ID:1615259

Simakov, Oleg ^[1]; Kawashima, Takeshi ^[2]; Marlétaz, Ferdinand ^[3]; Jenkins, Jerry ^[4]; Koyanagi, Ryo ^[2]; Mitros, Therese ^[5]; Hisata, Kanako ^[2]; Bredeson, Jessen ^[5]; Shoguchi, Eiichi ^[2]; Gyoja, Fuki ^[2]; Yue, Jia-Xing ^[6]; Chen, Yi-Chih ^[7]; Freeman, Robert M. ^[8]; Sasaki, Akane ^[9]; Hikosaka-Katayama, Tomoe ^[10]; Sato, Atsuko ^[11]; Fujie, Manabu ^[2]; Baughman, Kenneth W. ^[2]; Levine, Judith ^[12]; Gonzalez, Paul ^[12] more »

Okinawa Inst. of Science and Technology Graduate Univ., Onna, Okinawa (Japan); Univ. of Heidelberg, Heidelberg (Germany)
Okinawa Inst. of Science and Technology Graduate Univ., Onna, Okinawa (Japan)
Univ. of Oxford (United Kingdom)
HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States)
Univ. of California, Berkeley, CA (United States)
Rice Univ., Houston, TX (United States)
Academia Sinica, Taipei (Taiwan). Inst. of Cellular and Organismic Biology
Harvard Medical School, Boston, MA (United States)
Hiroshima Univ., Hiroshima (Japan). Marine Biological Lab.
Hiroshima Univ., Hiroshima (Japan). Natural Science Center for Basic Research and Development, Gene Science Division
Marine Biological Association of the UK, Plymouth (United Kingdom)
Stanford Univ., Pacific Grove, CA (United States). Hopkins Marine Station
Univ. of Montreal, QC (Canada)
Univ. of North Carolina, Chapel Hill, NC (United States)
Baylor College of Medicine, Houston, TX (United States). Human Genome Sequencing Center
Univ. of Cambridge (United Kingdom)
Univ. of Hawaii, Honolulu, HI (United States). Inst. for Biogenesis Research
National Inst. of Genetics, Mishima, Shizuoka (Japan)
Okinawa Inst. of Science and Technology Graduate Univ., Onna, Okinawa (Japan); Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Acorn worms, also known as enteropneust (literally, ‘gut-breathing’) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal ‘gill’ slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); NR01HD073104ational Institutes of Health (NIH); USPHS; National Aeronautics and Space Administration (NASA); MEXT Japan; OIST Japan

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1615259

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7579 Vol. 527; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Phylogenomic Resolution of the Hemichordate and Echinoderm Clade Cannon, Johanna T.; Kocot, Kevin M.; Waits, Damien S. Current Biology, Vol. 24, Issue 23 https://doi.org/10.1016/j.cub.2014.10.016	journal	December 2014
Sequencing and analysis of the transcriptome of the acorn worm Ptychodera flava, an indirect developing hemichordate Chen, Shu-Hwa; Li, Kun-Lin; Lu, I-Hsuan Marine Genomics, Vol. 15 https://doi.org/10.1016/j.margen.2014.04.010	journal	June 2014
Chordate Evolution in a New Light Tautz, Diethard Cell, Vol. 113, Issue 7 https://doi.org/10.1016/s0092-8674(03)00472-0	journal	June 2003
Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida Bourlat, Sarah J.; Juliusdottir, Thorhildur; Lowe, Christopher J. Nature, Vol. 444, Issue 7115 https://doi.org/10.1038/nature05241	journal	October 2006
A transposon-based chromosomal engineering method to survey a large cis-regulatory landscape in mice Kokubu, Chikara; Horie, Kyoji; Abe, Koichiro Nature Genetics, Vol. 41, Issue 8 https://doi.org/10.1038/ng.397	journal	July 2009
De novo identification of repeat families in large genomes Price, A. L.; Jones, N. C.; Pevzner, P. A. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1018	journal	June 2005
CDD: NCBI's conserved domain database Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1221	journal	November 2014
Assessing the root of bilaterian animals with scalable phylogenomic methods Hejnol, Andreas; Obst, Matthias; Stamatakis, Alexandros Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1677 https://doi.org/10.1098/rspb.2009.0896	journal	September 2009
Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints Irimia, M.; Tena, J. J.; Alexis, M. S. Genome Research, Vol. 22, Issue 12 https://doi.org/10.1101/gr.139725.112	journal	June 2012
Whole-Genome Sequence Assembly for Mammalian Genomes: Arachne 2 Jaffe, D. B. Genome Research, Vol. 13, Issue 1 https://doi.org/10.1101/gr.828403	journal	January 2003
Evolutionary history of the alpha2,8-sialyltransferase (ST8Sia) gene family: Tandem duplications in early deuterostomes explain most of the diversity found in the vertebrate ST8Sia genes Harduin-Lepers, Anne; Petit, Daniel; Mollicone, Rosella BMC Evolutionary Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2148-8-258	journal	January 2008
Endostyle-like Features of the Dorsal Epibranchial Ridge of an Enteropneust and the Hypothesis of Dorsal-Ventral Axis Inversion in Chordates Ruppert, Edward E.; Cameron, Christopher B.; Frick, Jennifer E. Invertebrate Biology, Vol. 118, Issue 2 https://doi.org/10.2307/3227061	journal	April 1999
Man is but a worm: Chordate origins Brown, Federico D.; Prendergast, Andrew; Swalla, Billie J. genesis, Vol. 46, Issue 11 https://doi.org/10.1002/dvg.20471	journal	November 2008
Genomic organization of Hox and ParaHox clusters in the echinoderm, A canthaster planci: SEA STAR HOX AND PARAHOX CLUSTERS Baughman, Kenneth W.; McDougall, Carmel; Cummins, Scott F. genesis, Vol. 52, Issue 12 https://doi.org/10.1002/dvg.22840	journal	November 2014
Unusual gene order and organization of the sea urchin hox cluster Cameron, R. Andrew; Rowen, Lee; Nesbitt, Ryan Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 306B, Issue 1 https://doi.org/10.1002/jez.b.21070	journal	January 2006
The Phylogenetic Position of the Pterobranch Hemichordates Based on 18S rDNA Sequence Data Halanych, Kenneth M. Molecular Phylogenetics and Evolution, Vol. 4, Issue 1 https://doi.org/10.1006/mpev.1995.1007	journal	March 1995
Comparative analysis of the genomic organization of Pax9 and its conserved physical association with Nkx2-9 in the human, mouse, and pufferfish genomes Santagati, Fabio; Gerber, Josef-Karl; Blusch, Jürgen H. Mammalian Genome, Vol. 12, Issue 3 https://doi.org/10.1007/s003350010267	journal	March 2001
Higher-level metazoan relationships: recent progress and remaining questions Edgecombe, Gregory D.; Giribet, Gonzalo; Dunn, Casey W. Organisms Diversity & Evolution, Vol. 11, Issue 2 https://doi.org/10.1007/s13127-011-0044-4	journal	March 2011
Anteroposterior Patterning in Hemichordates and the Origins of the Chordate Nervous System Lowe, Christopher J.; Wu, Mike; Salic, Adrian Cell, Vol. 113, Issue 7 https://doi.org/10.1016/S0092-8674(03)00469-0	journal	June 2003
Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution Ulitsky, Igor; Shkumatava, Alena; Jan, Calvin H. Cell, Vol. 147, Issue 7 https://doi.org/10.1016/j.cell.2011.11.055	journal	December 2011
Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution Ulitsky, Igor; Shkumatava, Alena; Jan, Calvin H. Cell, Vol. 151, Issue 3 https://doi.org/10.1016/j.cell.2012.10.002	journal	October 2012
Identical Genomic Organization of Two Hemichordate Hox Clusters Freeman, Robert; Ikuta, Tetsuro; Wu, Michael Current Biology, Vol. 22, Issue 21 https://doi.org/10.1016/j.cub.2012.08.052	journal	November 2012
Whole-Body Acoel Regeneration Is Controlled by Wnt and Bmp-Admp Signaling Srivastava, Mansi; Mazza-Curll, Kathleen L.; van Wolfswinkel, Josien C. Current Biology, Vol. 24, Issue 10 https://doi.org/10.1016/j.cub.2014.03.042	journal	May 2014
An Integrated Holo-Enhancer Unit Defines Tissue and Gene Specificity of the Fgf8 Regulatory Landscape Marinić, Mirna; Aktas, Tugce; Ruf, Sandra Developmental Cell, Vol. 24, Issue 5 https://doi.org/10.1016/j.devcel.2013.01.025	journal	March 2013
Hemichordates and the origin of chordates Gerhart, John; Lowe, Christopher; Kirschner, Marc Current Opinion in Genetics & Development, Vol. 15, Issue 4 https://doi.org/10.1016/j.gde.2005.06.004	journal	August 2005
Up-regulation of C/EBP by thyroid hormones: A case demonstrating the vertebrate-like thyroid hormone signaling pathway in amphioxus Wang, Shaohui; Zhang, Shicui; Zhao, Bosheng Molecular and Cellular Endocrinology, Vol. 313, Issue 1-2 https://doi.org/10.1016/j.mce.2009.08.024	journal	December 2009
Maternal Oct1/2 is required for Nodal and Vg1/Univin expression during dorsal–ventral axis specification in the sea urchin embryo Range, Ryan; Lepage, Thierry Developmental Biology, Vol. 357, Issue 2 https://doi.org/10.1016/j.ydbio.2011.07.005	journal	September 2011
Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes Ruiz-Trillo, Iñaki; Riutort, Marta; Fourcade, H. Matthew Molecular Phylogenetics and Evolution, Vol. 33, Issue 2 https://doi.org/10.1016/j.ympev.2004.06.002	journal	November 2004
The amphioxus genome and the evolution of the chordate karyotype Putnam, Nicholas H.; Butts, Thomas; Ferrier, David E. K. Nature, Vol. 453, Issue 7198 https://doi.org/10.1038/nature06967	journal	June 2008
Acoelomorph flatworms are deuterostomes related to Xenoturbella Philippe, Hervé; Brinkmann, Henner; Copley, Richard R. Nature, Vol. 470, Issue 7333 https://doi.org/10.1038/nature09676	journal	February 2011
Comparative population genomics in animals uncovers the determinants of genetic diversity Romiguier, J.; Gayral, P.; Ballenghien, M. Nature, Vol. 515, Issue 7526 https://doi.org/10.1038/nature13685	journal	August 2014
Scenarios for the making of vertebrates Holland, Nicholas D.; Holland, Linda Z.; Holland, Peter W. H. Nature, Vol. 520, Issue 7548 https://doi.org/10.1038/nature14433	journal	April 2015
The deuterostome context of chordate origins Lowe, Christopher J.; Clarke, D. Nathaniel; Medeiros, Daniel M. Nature, Vol. 520, Issue 7548 https://doi.org/10.1038/nature14434	journal	April 2015
TGFβ signalling in context Massagué, Joan Nature Reviews Molecular Cell Biology, Vol. 13, Issue 10 https://doi.org/10.1038/nrm3434	journal	September 2012
Transphyletic conservation of developmental regulatory state in animal evolution Royo, J. L.; Maeso, I.; Irimia, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1109037108	journal	August 2011
Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla Cameron, C. B.; Garey, J. R.; Swalla, B. J. Proceedings of the National Academy of Sciences, Vol. 97, Issue 9 https://doi.org/10.1073/pnas.97.9.4469	journal	April 2000
Deciphering deuterostome phylogeny: molecular, morphological, and palaeontological perspectives Smith, Andrew B.; Swalla, Billie J. Animal Evolution https://doi.org/10.1093/acprof:oso/9780199549429.003.0009	book	August 2009
Gene prediction with a hidden Markov model and a new intron submodel Stanke, M.; Waack, S. Bioinformatics, Vol. 19, Issue Suppl 2 https://doi.org/10.1093/bioinformatics/btg1080	journal	September 2003
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating Lartillot, Nicolas; Lepage, Thomas; Blanquart, Samuel Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp368	journal	June 2009
Identification of Cis-regulatory Elements in the Mouse Pax9/Nkx2-9 Genomic Region: Implication for Evolutionary Conserved Synteny Santagati, Fabio; Abe, Kuniya; Schmidt, Volker Genetics, Vol. 165, Issue 1 https://doi.org/10.1093/genetics/165.1.235	journal	September 2003
The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach Harduin-Lepers, Anne; Mollicone, Rosella; Delannoy, Philippe Glycobiology, Vol. 15, Issue 8 https://doi.org/10.1093/glycob/cwi063	journal	April 2005
Comparison of Pax1/9 Locus Reveals 500-Myr-Old Syntenic Block and Evolutionary Conserved Noncoding Regions Wang, Wei; Zhong, Jing; Su, Bing Molecular Biology and Evolution, Vol. 24, Issue 3 https://doi.org/10.1093/molbev/msl205	journal	December 2006
Ancient Vertebrate Conserved Noncoding Elements Have Been Evolving Rapidly in Teleost Fishes Lee, A. P.; Kerk, S. Y.; Tan, Y. Y. Molecular Biology and Evolution, Vol. 28, Issue 3 https://doi.org/10.1093/molbev/msq304	journal	November 2010
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
VISTA Enhancer Browser--a database of tissue-specific human enhancers Visel, A.; Minovitsky, S.; Dubchak, I. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl822	journal	January 2007
Ensembl 2015 Cunningham, Fiona; Amode, M. Ridwan; Barrell, Daniel Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1010	journal	October 2014
A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network Gillis, J. Andrew; Fritzenwanker, Jens H.; Lowe, Christopher J. Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1727 https://doi.org/10.1098/rspb.2011.0599	journal	June 2011
Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives Swalla, Billie J.; Smith, Andrew B. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1496 https://doi.org/10.1098/rstb.2007.2246	journal	January 2008
Ab initio Gene Finding in Drosophila Genomic DNA Salamov, Asaf A.; Solovyev, Victor V. Genome Research, Vol. 10, Issue 4, p. 516-522 https://doi.org/10.1101/gr.10.4.516	journal	April 2000
Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads Kajitani, Rei; Toshimoto, Kouta; Noguchi, Hideki Genome Research, Vol. 24, Issue 8 https://doi.org/10.1101/gr.170720.113	journal	April 2014
The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures: PROTOGLOSSUS FILTER-FEEDING STRUCTURES Gonzalez, Paul; Cameron, Christopher B. Biological Journal of the Linnean Society, Vol. 98, Issue 4 https://doi.org/10.1111/j.1095-8312.2009.01332.x	journal	November 2009
Fine Structure and Function of Pharynx Cilia in Glossobalanus minutus Kowalewsky (Enteropneusta) Pardos, Fernando Acta Zoologica, Vol. 69, Issue 1 https://doi.org/10.1111/j.1463-6395.1988.tb00895.x	journal	March 1988
The Genome of the Sea Urchin Strongylocentrotus purpuratus Sodergren, E.; Weinstock, G. M.; Davidson, E. H. Science, Vol. 314, Issue 5801 https://doi.org/10.1126/science.1133609	journal	November 2006
Repbase Update, a database of eukaryotic repetitive elements Jurka, J.; Kapitonov, V. V.; Pavlicek, A. Cytogenetic and Genome Research, Vol. 110, Issue 1-4 https://doi.org/10.1159/000084979	journal	January 2005
The genome of the sea urchin Strongylocentrotus purpuratus. Consortium, Sea Urchin Genome Sequencing; Sodergren, Erica; Weinstock, George M. Carnegie Mellon University https://doi.org/10.1184/r1/6104471	text	January 2006
A detailed description of the development of the hemichordate Saccoglossus kowalevskii using SEM, TEM, Histology and 3D-reconstructions Kaul-Strehlow, Sabrina; Stach, Thomas Frontiers in Zoology, Vol. 10, Issue 1 https://doi.org/10.1186/1742-9994-10-53	journal	January 2013
Cis-regulatory analysis of nodal and maternal control of dorsal-ventral axis formation by Univin, a TGF- related to Vg1 Range, R.; Lapraz, F.; Quirin, M. Development, Vol. 134, Issue 20 https://doi.org/10.1242/dev.007799	journal	September 2007
Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: insight into function and evolution of the pharyngeal epithelium Ogasawara, Michio; Wada, Hiroshi; Peters, Heiko Development, Vol. 126, Issue 11 https://doi.org/10.1242/dev.126.11.2539	journal	June 1999
Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution Lowe, Christopher J.; Terasaki, Mark; Wu, Michael PLoS Biology, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pbio.0040291	journal	August 2006
New Insights on the Sialidase Protein Family Revealed by a Phylogenetic Analysis in Metazoa Giacopuzzi, Edoardo; Bresciani, Roberto; Schauer, Roland PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0044193	journal	August 2012
The Genome of the Sea Urchin Strongylocentrotus purpuratus I., Arnone, M.; A., Cameron, R.; C., Angerer, R. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/txak-zc02	text	January 2006
A cDNA Resource for Gene Expression Studies of a Hemichordate, Ptychodera flava Tagawa, Kuni; Arimito, Asuka; Sasaki, Akane Zoological Science, Vol. 31, Issue 7 https://doi.org/10.2108/zs130262	journal	July 2014
The History of Balanoglossus and Tornaria Agassiz, Alexander Memoirs of the American Academy of Arts and Sciences, Vol. 9, Issue 2 https://doi.org/10.2307/25058009	journal	January 1873

Cited By (51)

Phylogenetic Distribution of CMP-Neu5Ac Hydroxylase (CMAH), the Enzyme Synthetizing the Proinflammatory Human Xenoantigen Neu5Gc Peri, Sateesh; Kulkarni, Asmita; Feyertag, Felix Genome Biology and Evolution, Vol. 10, Issue 1 https://doi.org/10.1093/gbe/evx251	journal	December 2017
JmjC Domain-Encoding Genes Are Conserved in Highly Regenerative Metazoans and Are Associated with Planarian Whole-Body Regeneration Cao, Ping-Lin; Kumagai, Nobuyoshi; Inoue, Takeshi Genome Biology and Evolution, Vol. 11, Issue 2 https://doi.org/10.1093/gbe/evz021	journal	February 2019
Deuterostome Genomics: Lineage-Specific Protein Expansions That Enabled Chordate Muscle Evolution Inoue, Jun; Satoh, Noriyuki Molecular Biology and Evolution, Vol. 35, Issue 4 https://doi.org/10.1093/molbev/msy002	journal	January 2018
Emergence of a Thrombospondin Superfamily at the Origin of Metazoans Shoemark, Deborah K.; Ziegler, Berenice; Watanabe, Hiroshi Molecular Biology and Evolution, Vol. 36, Issue 6 https://doi.org/10.1093/molbev/msz060	journal	March 2019
Grafting or Pruning in the Animal Tree: Lateral Gene Transfer and Gene Loss? Hotopp, Julie C. Dunning bioRxiv https://doi.org/10.1101/229468	posted_content	December 2017
The genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle Leclère, Lucas; Horin, Coralie; Chevalier, Sandra https://doi.org/10.1101/369959	posted_content	July 2018
Existence and functions of hypothalamic kisspeptin neuropeptide signaling system in a non-chordate deuterostome species Wang, Tianming; Cao, Zheng; Shen, Zhangfei https://doi.org/10.1101/851261	preprint	January 2019
A phylogenomic resolution of the sea urchin tree of life Mongiardino Koch, Nicolás; Coppard, Simon E.; Lessios, Harilaos A. BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1300-4	journal	December 2018
The sea cucumber genome provides insights into morphological evolution and visceral regeneration Zhang, Xiaojun; Sun, Lina; Yuan, Jianbo PLOS Biology, Vol. 15, Issue 10 https://doi.org/10.1371/journal.pbio.2003790	journal	October 2017
Greenlip Abalone ( Haliotis laevigata ) Genome and Protein Analysis Provides Insights into Maturation and Spawning Botwright, Natasha A.; Zhao, Min; Wang, Tianfang G3: Genes\|Genomes\|Genetics, Vol. 9, Issue 10 https://doi.org/10.1534/g3.119.400388	journal	August 2019
Evolution of Homeobox Gene Clusters in Animals: The Giga-Cluster and Primary vs. Secondary Clustering Ferrier, David E. K. Frontiers in Ecology and Evolution, Vol. 4 https://doi.org/10.3389/fevo.2016.00036	journal	April 2016
Ancient Origin of the CARD–Coiled Coil/Bcl10/MALT1-Like Paracaspase Signaling Complex Indicates Unknown Critical Functions Staal, Jens; Driege, Yasmine; Haegman, Mira Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.01136	journal	May 2018
Characterization of the TLR Family in Branchiostoma lanceolatum and Discovery of a Novel TLR22-Like Involved in dsRNA Recognition in Amphioxus Ji, Jie; Ramos-Vicente, David; Navas-Pérez, Enrique Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.02525	journal	November 2018
Role of the Extremolytes Ectoine and Hydroxyectoine as Stress Protectants and Nutrients: Genetics, Phylogenomics, Biochemistry, and Structural Analysis Czech, Laura; Hermann, Lucas; Stöveken, Nadine Genes, Vol. 9, Issue 4 https://doi.org/10.3390/genes9040177	journal	March 2018
Family matters Mayer, Mark L.; Jegla, Timothy eLife, Vol. 7 https://doi.org/10.7554/elife.43815	journal	December 2018
Evolutionary emergence of Hairless as a novel component of the Notch signaling pathway Miller, Steven W.; Movsesyan, Artem; Zhang, Sui eLife, Vol. 8 https://doi.org/10.7554/elife.48115	journal	September 2019
Head regeneration in hemichordates is not a strict recapitulation of development Luttrell, Shawn M.; Gotting, Kirsten; Ross, Eric Developmental Dynamics, Vol. 245, Issue 12 https://doi.org/10.1002/dvdy.24457	journal	October 2016
Enhancer activities of amphioxus Brachyury genes in embryos of the ascidian, Ciona intestinalis Tominaga, Hitoshi; Satoh, Noriyuki; Ueno, Naoto genesis, Vol. 56, Issue 8 https://doi.org/10.1002/dvg.23240	journal	August 2018
Compartmentalized expression patterns of pancreatic- and gastric-related genes in the alimentary canal of the ascidian Ciona intestinalis: evolutionary insights into the functional regionality of the gastrointestinal tract in Olfactores Nakayama, Satoshi; Ogasawara, Michio Cell and Tissue Research, Vol. 370, Issue 1 https://doi.org/10.1007/s00441-017-2627-7	journal	May 2017
The evolutionary origin of chordate segmentation: revisiting the enterocoel theory Onai, Takayuki Theory in Biosciences, Vol. 137, Issue 1 https://doi.org/10.1007/s12064-018-0260-y	journal	February 2018
On the larva and the zooid of the pterobranch Rhabdopleura recondita Beli, Cameron and Piraino, 2018 (Hemichordata, Graptolithina) Strano, F.; Micaroni, V.; Beli, E. Marine Biodiversity, Vol. 49, Issue 4 https://doi.org/10.1007/s12526-018-0933-2	journal	January 2019
Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China) Han, Jian; Morris, Simon Conway; Ou, Qiang Nature, Vol. 542, Issue 7640 https://doi.org/10.1038/nature21072	journal	January 2017
The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest Hall, Michael R.; Kocot, Kevin M.; Baughman, Kenneth W. Nature, Vol. 544, Issue 7649 https://doi.org/10.1038/nature22033	journal	April 2017
Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads Luo, Yi-Jyun; Kanda, Miyuki; Koyanagi, Ryo Nature Ecology & Evolution, Vol. 2, Issue 1 https://doi.org/10.1038/s41559-017-0389-y	journal	December 2017
The genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle Leclère, Lucas; Horin, Coralie; Chevalier, Sandra Nature Ecology & Evolution, Vol. 3, Issue 5 https://doi.org/10.1038/s41559-019-0833-2	journal	March 2019
Reconstruction of the sialylation pathway in the ancestor of eukaryotes Petit, Daniel; Teppa, Elin; Cenci, Ugo Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-20920-1	journal	February 2018
De novo draft assembly of the Botrylloides leachii genome provides further insight into tunicate evolution Blanchoud, Simon; Rutherford, Kim; Zondag, Lisa Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23749-w	journal	April 2018
Toll-like receptor pathway evolution in deuterostomes Tassia, Michael G.; Whelan, Nathan V.; Halanych, Kenneth M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1617722114	journal	June 2017
BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates Su, Yi-Hsien; Chen, Yi-Chih; Ting, Hsiu-Chi Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1901919116	journal	June 2019
Draft genome of the Peruvian scallop Argopecten purpuratus Li, Chao; Liu, Xiao; Liu, Bo GigaScience, Vol. 7, Issue 4 https://doi.org/10.1093/gigascience/giy031	journal	April 2018
Evolutionary History of GLIS Genes Illuminates Their Roles in Cell Reprograming and Ciliogenesis Yasuoka, Yuuri; Matsumoto, Masahito; Yagi, Ken Molecular Biology and Evolution, Vol. 37, Issue 1 https://doi.org/10.1093/molbev/msz205	journal	September 2019
Who Let the CAT Out of the Bag? Accurately Dealing with Substitutional Heterogeneity in Phylogenomic Analyses Whelan, Nathan V.; Halanych, Kenneth M. Systematic Biology https://doi.org/10.1093/sysbio/syw084	journal	September 2016
The genome of the contractile demosponge Tethya wilhelma and the evolution of metazoan neural signalling pathways Francis, Warren R.; Eitel, Michael; Vargas, Sergio bioRxiv https://doi.org/10.1101/120998	posted_content	April 2017
Endoderm Morphogenesis Reveals Integration of Distinct Processes in the Development and Evolution of Pharyngeal Arches Okada, Kazunori; Wada, Hiroshi; Takada, Shinji bioRxiv https://doi.org/10.1101/260356	posted_content	February 2018
A phylogenomic resolution of the sea urchin tree of life Mongiardino Koch, Nicolás; Coppard, Simon E.; Lessios, Harilaos A. BMC Evolutionary Biology https://doi.org/10.1101/430595	posted_content	September 2018
Hairless as a novel component of the Notch signaling pathway Miller, Steven W.; Movsesyan, Artem; Zhang, Sui eLife https://doi.org/10.1101/621367	journal	April 2019
Urbilaterian origin and evolution of sNPF-type neuropeptide signalling Yañez-Guerra, Luis Alfonso; Zhong, Xingxing; Moghul, Ismail bioRxiv https://doi.org/10.1101/712687	posted_content	July 2019
Concordant developmental expression profiles of orthologues in highly divergent Bilateria Ferretti, Luca; Krämer-Eis, Andrea; Schiffer, Philipp H. https://doi.org/10.1101/786723	preprint	September 2019
Phylogenetic inference identifies two eumetazoan TRPM clades and an 8 ^th family of TRP channel, TRP soromelastatin (TRPS) Himmel, Nathaniel J.; Gray, Thomas R.; Cox, Daniel N. Molecular Biology and Evolution https://doi.org/10.1101/860445	posted_content	November 2019
Regeneration in the enteropneust hemichordate, Ptychodera flava , and its evolutionary implications Arimoto, Asuka; Tagawa, Kuni Development, Growth & Differentiation, Vol. 60, Issue 6 https://doi.org/10.1111/dgd.12557	journal	July 2018
The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity Holzer, Astrid S.; Bartošová-Sojková, Pavla; Born-Torrijos, Ana Molecular Ecology, Vol. 27, Issue 7 https://doi.org/10.1111/mec.14558	journal	April 2018
Evolution of the angiopoietin-like gene family in teleosts and their role in skin regeneration Costa, Rita A.; Cardoso, João C. R.; Power, Deborah M. BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-016-0859-x	journal	January 2017
Two more Posterior Hox genes and Hox cluster dispersal in echinoderms Szabó, Réka; Ferrier, David E. K. BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1307-x	journal	December 2018
Grafting or pruning in the animal tree: lateral gene transfer and gene loss? Dunning Hotopp, Julie C. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4832-5	journal	June 2018
Cambrian suspension-feeding tubicolous hemichordates Nanglu, Karma; Caron, Jean-Bernard; Conway Morris, Simon BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0271-4	journal	July 2016
Human transposable elements in Repbase: genomic footprints from fish to humans Kojima, Kenji K. Mobile DNA, Vol. 9, Issue 1 https://doi.org/10.1186/s13100-017-0107-y	journal	January 2018
The chordate ancestor possessed a single copy of the Brachyury gene for notochord acquisition Inoue, Jun; Yasuoka, Yuuri; Takahashi, Hiroki Zoological Letters, Vol. 3, Issue 1 https://doi.org/10.1186/s40851-017-0064-9	journal	March 2017
Development of the thyroid gland Nilsson, Mikael; Fagman, Henrik Development, Vol. 144, Issue 12 https://doi.org/10.1242/dev.145615	journal	June 2017
Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens Mayorova, Tatiana D.; Tian, Shi; Cai, Weigang Frontiers in Neuroscience, Vol. 10 https://doi.org/10.3389/fnins.2016.00553	journal	December 2016
Signalling by Transforming Growth Factor Beta Isoforms in Wound Healing and Tissue Regeneration Gilbert, Richard; Vickaryous, Matthew; Viloria-Petit, Alicia Journal of Developmental Biology, Vol. 4, Issue 2 https://doi.org/10.3390/jdb4020021	journal	June 2016
Metazoan evolution of glutamate receptors reveals unreported phylogenetic groups and divergent lineage-specific events Ramos-Vicente, David; Ji, Jie; Gratacòs-Batlle, Esther eLife, Vol. 7 https://doi.org/10.7554/elife.35774	journal	November 2018