A New Spiralian Phylogeny Places the Enigmatic Arrow Worms among Gnathiferans
Open accessAbstract
Chaetognaths (arrow worms) are an enigmatic group of marine animals whose phylogenetic position remains elusive, in part because they display a mix of developmental and morphological characters associated with other groups [1, 2]. In particular, it remains unclear whether they are a sister group to protostomes [1, 2], one of the principal animal superclades, or whether they bear a closer relationship with some spiralian phyla [3, 4]. Addressing the phylogenetic position of chaetognaths and refining our understanding of relationships among spiralians are essential to fully comprehend character changes during bilaterian evolution [5]. To tackle these questions, we generated new transcriptomes for ten chaetognath species, compiling an extensive phylogenomic dataset that maximizes data occupancy and taxonomic representation. We employed inference methods that consider rate and compositional heterogeneity across taxa to avoid limitations of earlier analyses [6]. In this way, we greatly improved the resolution of the protostome tree of life. We find that chaetognaths cluster together with rotifers, gnathostomulids, and micrognathozoans within an expanded Gnathifera clade and that this clade is the sister group to other spiralians [7, 8]. Our analysis shows that several previously proposed groupings are likely due to systematic error, and we propose a revised organization of Lophotrochozoa with three main clades: Tetraneuralia (mollusks and entoprocts), Lophophorata (brachiopods, phoronids, and ectoprocts), and a third unnamed clade gathering annelids, nemerteans, and platyhelminthes. Consideration of classical morphological, developmental, and genomic characters in light of this topology indicates secondary loss as a fundamental trend in spiralian evolution.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
CAT/CATGTR offers improved resilience to long-branch attraction artefacts and is almost always better fitting than standard site-homogeneous amino acid substitution models.
“CAT/CATGTR offers improved resilience to long-branch attraction artefacts (LBA)22 and is almost always better fitting than standard site-homogeneous amino acid substitution models (e.g. WAG)8–10,23–29.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [25]
Cites
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291 · see citing works
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msu300 · Cited by 26,046 · see citing works
Full-length transcriptome assembly from RNA-Seq data without a reference genome
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1883 · Cited by 20,776 · see citing works
Near-optimal probabilistic RNA-seq quantification
Bray, N. L., Pimentel, H., Melsted, P., & Pachter, L. (2016) · Nature Biotechnology · doi:10.1038/nbt.3519 · Cited by 9,723 · see citing works
Haas, B. J., Salzberg, S. L., Zhu, W., Pertea, M., Allen, J., Orvis, J., White, O. R., Buell, C. R., & Wortman, J. R. (2008) · Genome biology · doi:10.1186/gb-2008-9-1-r7 · Cited by 4,051 · see citing works
Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · cited 3× · see citing works
“Many early phylogenomic studies recovered a ‘Platyzoa’ clade that collected many morphologically-simple fast-evolving lineages, including platyhelminthes, rotifers, gastrotrichs, gnathostomulids and others [4].”
Criscuolo, A., & Gribaldo, S. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-210 · Cited by 1,607 · see citing works
A revised six-kingdom system of life
Cavalier‐Smith, T. (1998) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s0006323198005167 · Cited by 1,067 · see citing works
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
Phylogenomics: The beginning of incongruence?
JEFFROY, O., BRINKMANN, H., DELSUC, F., & PHILIPPE, H. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.003 · Cited by 698 · see citing works
Corset: enabling differential gene expression analysis for
Davidson, N., & Oshlack, A. (2014) · Genome biology · doi:10.1186/s13059-014-0410-6 · Cited by 677 · see citing works
The African coelacanth genome provides insights into tetrapod evolution
Amemiya, C. T., Alföldi, J., Lee, A., Fan, S., Philippe, H., MacCallum, I., Braasch, I., Manousaki, T., Schneider, I., Rohner, N., et al. (2013) · Nature · doi:10.1038/nature12027 · Cited by 660 · see citing works
Insights into bilaterian evolution from three spiralian genomes
Simakov, O., Marletaz, F., Cho, S.-J., Edsinger-Gonzales, E., Havlak, P., Hellsten, U., Kuo, D.-H., Larsson, T., Lv, J., Arendt, D., et al. (2013) · Nature · doi:10.1038/nature11696 · Cited by 656 · see citing works
Self-citationThe origins and relationships of lower invertebrates
Morris, S. C. (1983) · Lethaia · doi:10.1111/j.1502-3931.1983.tb02002.x · Cited by 605 · see citing works
Acoelomorph flatworms are deuterostomes related to Xenoturbella
Philippe, H., Brinkmann, H., Copley, R. R., Moroz, L. L., Nakano, H., Poustka, A. J., Wållberg, A., Peterson, K. J., & Telford, M. J. (2011) · Nature · doi:10.1038/nature09676 · Cited by 432 · see citing works
Xenacoelomorpha is the sister group to Nephrozoa
Cannon, J. T., Vellutini, B. C., Smith, J., Ronquist, F., Jondelius, U., & Hejnol, A. (2016) · Nature · doi:10.1038/nature16520 · Cited by 364 · see citing works
Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals
Feuda, R., Dohrmann, M., Pett, W., Philippe, H., Rota-Stabelli, O., Lartillot, N., Wörheide, G., & Pisani, D. (2017) · Current Biology · doi:10.1016/j.cub.2017.11.008 · Cited by 291 · see citing works
Spiralian Phylogeny Informs the Evolution of Microscopic Lineages
Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sørensen, M. V., Kristensen, R. M., Hejnol, A., Dunn, C. W., Giribet, G., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.068 · Cited by 278 · see citing works
Hemichordate genomes and deuterostome origins
Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J. W., Koyanagi, R., Mitros, T., Hisata, K., Bredeson, J. V., Shoguchi, E., Gyoja, F., et al. (2015) · Nature · doi:10.1038/nature16150 · Cited by 250 · see citing works
Self-citationLiu, Y., Schmidt, B., & Maskell, D. L. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq338 · Cited by 234 · see citing works
Phylogenomic Insights into Animal Evolution
Telford, M. J., Budd, G. E., & Philippe, H. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.060 · Cited by 213 · see citing works
Phylogenomics of Lophotrochozoa with Consideration of Systematic Error
Kocot, K. M., Struck, T. H., Merkel, J., Waits, D. S., Todt, C., Brannock, P. M., Weese, D., Cannon, J. T., Moroz, L. L., Lieb, B., et al. (2016) · Systematic Biology · doi:10.1093/sysbio/syw079 · Cited by 204 · see citing works
Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans
Fröbius, A. C., & Funch, P. (2017) · Nature Communications · doi:10.1038/s41467-017-00020-w · Cited by 198 · see citing works
Convergent evolution of bilaterian nerve cords
Martín-Durán, J. M., Pang, K., Børve, A., Semmler, H., Furu, A., Cannon, J. T., Jondelius, U., & Hejnol, A. (2017) · Nature · doi:10.1038/nature25030 · Cited by 190 · see citing works
Algorithm of OMA for large-scale orthology inference
Roth, A. C., Gonnet, G. H., & Dessimoz, C. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-518 · Cited by 180 · see citing works
On Reduced Amino Acid Alphabets for Phylogenetic Inference
Susko, E., & Roger, A. J. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm144 · Cited by 177 · see citing works
Platyzoan Paraphyly Based on Phylogenomic Data Supports a Noncoelomate Ancestry of Spiralia
Struck, T. H., Wey-Fabrizius, A. R., Golombek, A., Hering, L., Weigert, A., Bleidorn, C., Klebow, S., Iakovenko, N., Hausdorf, B., Petersen, M., et al. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu143 · Cited by 177 · see citing works
Riedl, R. J. M. (1969) · Science · doi:10.1126/science.163.3866.445 · Cited by 149 · see citing works
The phylogenetic affinities of the chaetognaths: a molecular analysis.
Telford, M. J., & Holland, P. W. H. (1993) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040030 · Cited by 138 · see citing works
Broad taxon and gene sampling indicate that chaetognaths are protostomes
Matus, D. Q., Copley, R. R., Dunn, C. W., Hejnol, A., Eccleston, H., Halanych, K. M., Martindale, M. Q., & Telford, M. J. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.017 · Cited by 138 · see citing works
Chaetognath phylogenomics: a protostome with deuterostome-like development
Marlétaz, F., Martin, E., Perez, Y., Papillon, D., Caubit, X., Lowe, C. J., Freeman, B., Fasano, L., Dossat, C., Wincker, P., et al. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.016 · Cited by 138 · see citing works
Self-citationAssembling the lophotrochozoan (=spiralian) tree of life
Giribet, G. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2241 · Cited by 138 · see citing works
Vestigial prototroch in a basal nemertean,Carinoma tremaphoros(Nemertea; Palaeonemertea)
Maslakova, S. A., Martindale, M. Q., & Norenburg, J. L. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04027.x · Cited by 132 · see citing works
Ahlrichs, W. H. (1997) · Zoomorphology · doi:10.1007/s004350050028 · Cited by 130 · see citing works
A Twist in Time--The Evolution of Spiral Cleavage in the Light of Animal Phylogeny
Hejnol, A. (2010) · Integrative and Comparative Biology · doi:10.1093/icb/icq103 · Cited by 117 · see citing works
Sister-Group Relationship of Gnathostomulida and Rotifera-Acanthocephala
Rieger, R. M., & Tyler, S. (1995) · Invertebrate Biology · doi:10.2307/3226891 · Cited by 106 · see citing works
Wanninger, A. (2009) · Biological Bulletin · doi:10.1086/bblv216n3p293 · Cited by 105 · see citing works
Deuterostomic Development in the Protostome Priapulus caudatus
Martín-Durán, J. M., Janßen, R., Wennberg, S. A., Budd, G. E., & Hejnol, A. (2012) · Current Biology · doi:10.1016/j.cub.2012.09.037 · Cited by 95 · see citing works
Simion, P., Belkhir, K., Francois, C. M., Veyssier, J., Rink, J. C., Manuel, M., Philippe, H., & Telford, M. J. (2018) · BMC Biology · doi:10.1186/s12915-018-0486-7 · Cited by 95 · see citing works
Sørensen, M. V. (2002) · Journal of Morphology · doi:10.1002/jmor.10038 · Cited by 89 · see citing works
Chætognath transcriptome reveals ancestral and unique features among bilaterians
Marlétaz, F., André Gilles, A., Caubit, X., Perez, Y., Dossat, C., Samain, S., Gyapay, G., Wincker, P., & Parco, Y. L. (2008) · Genome biology · doi:10.1186/gb-2008-9-6-r94 · Cited by 86 · see citing works
Self-citationPhylogenetic Position of Nemertea Derived from Phylogenomic Data
Struck, T. H., & Fisse, F. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn019 · Cited by 86 · see citing works
Site-heterogeneous mutation-selection models within the PhyloBayes-MPI package
Rodrigue, N., & Lartillot, N. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt729 · Cited by 74 · see citing works
The structure and composition of the teeth and grasping spines of chaetognaths
Bone, Q., Ryan, K. P., & Pulsford, A. L. (1983) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315400071332 · Cited by 50 · see citing works
Hox gene survey in the chaetognath Spadella cephaloptera: evolutionary implications
Papillon, D., Perez, Y., Fasano, L., Parco, Y. L., & Caubit, X. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0306-z · Cited by 41 · see citing works
Papillon, D., Perez, Y., Caubit, X., & Parco, Y. L. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.12.004 · Cited by 36 · see citing works
A Large Cambrian Chaetognath with Supernumerary Grasping Spines
Briggs, D. E. G., & Caron, J. (2017) · Current Biology · doi:10.1016/j.cub.2017.07.003 · Cited by 27 · see citing works
Gasmi, S., Nve, G., Pech, N., Tekaya, S., André Gilles, A., & Perez, Y. (2014) · Frontiers in Zoology · doi:10.1186/s12983-014-0084-7 · Cited by 23 · see citing works
Who Needs Sex (or Males) Anyway?
Gross, L. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050099 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 50 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
NCBI Taxonomy: a comprehensive update on curation, resources and tools
Schoch, C. L., Ciufo, S., Domrachev, M., Hotton, C. L., Kannan, S., Khovanskaya, R., Leipe, D., Mcveigh, R., O’Neill, K., Robbertse, B., et al. (2020) · Database · doi:10.1093/database/baaa062 · Cited by 2,635 · see citing works
Revisiting metazoan phylogeny with genomic sampling of all phyla
Laumer, C. E., Fernández, R., Lemer, S., Combosch, D., Kocot, K. M., Riesgo, A., Andrade, S. C. S., Sterrer, W., Sørensen, M. V., & Giribet, G. (2019) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2019.0831 · Cited by 360 · see citing works
3D genomics across the tree of life identifies condensin II as a determinant of architecture type
Hoencamp, C., Dudchenko, O., Elbatsh, A., Brahmachari, S., Raaijmakers, J., van Schaik, T., Cacciatore, Á. S., Contessoto, V. G., van Heesbeen, R. V., van den Broek, B., et al. (2021) · Science · doi:10.1126/science.abe2218 · Cited by 205 · see citing works
Monroig, Ó., Shu‐Chien, A. C., Kabeya, N., Tocher, D. R., & Castro, L. F. C. (2022) · Progress in Lipid Research · doi:10.1016/j.plipres.2022.101157 · Cited by 216 · see citing works
The ‘biomineralization toolkit’ and the origin of animal skeletons
Murdock, D. J. E. (2020) · Biological Reviews · doi:10.1111/brv.12614 · Cited by 177 · see citing works
Gene gain and loss across the metazoan tree of life
Fernández, R., & Gabaldón, T. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-019-1069-x · Cited by 165 · see citing works
OMA standalone: orthology inference among public and custom genomes and transcriptomesPreprint
Altenhoff, A., Levy, J., Zarowiecki, M., Tomiczek, B., Vesztrocy, A. W., Dalquen, D. A., Müller, S., Telford, M. J., Glover, N. M., Dylus, D., et al. (2019) · Genome Research · doi:10.1101/gr.243212.118 · Cited by 159 · see citing works
Philippe, H., Poustka, A. J., Chiodin, M., Hoff, K. J., Dessimoz, C., Tomiczek, B., Schiffer, P. H., Müller, S., Domman, D., Horn, M., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.04.009 · Cited by 152 · see citing works
Self-citationRedmond, A. K., & McLysaght, A. (2021) · Nature Communications · doi:10.1038/s41467-021-22074-7 · Cited by 139 · see citing works
The evolution of insect biodiversity
Tihelka, E., Cai, C., Giacomelli, M., Lozano-Fernández, J., Rota‐Stabelli, O., Huang, D., Engel, M. S., Donoghue, P. C. J., & Pisani, D. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.057 · Cited by 138 · see citing works
The hagfish genome and the evolution of vertebrates
Marlétaz, F., Timoshevskaya, N. Y., Timoshevskiy, V. A., Parey, E., Simakov, O., Gavriouchkina, D., Suzuki, M., Kubokawa, K., Brenner, S., Smith, J. J., et al. (2024) · Nature · doi:10.1038/s41586-024-07070-3 · Cited by 126 · see citing works
Self-citationThe Scaly-foot Snail genome and implications for the origins of biomineralised armour
Sun, J., Chen, C., Miyamoto, N., Li, R.-S., Sigwart, J., Xu, T., Sun, Y.-N., Wong, W.-C., Ip, J. C., Zhang, W., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15522-3 · Cited by 113 · see citing works
Widespread patterns of gene loss in the evolution of the animal kingdom
Guijarro-Clarke, C., Holland, P. W. H., & Paps, J. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1129-2 · Cited by 122 · see citing works
Phylogenomic Subsampling and the Search for Phylogenetically Reliable Loci
Koch, N. M. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab151 · Cited by 121 · see citing works
Ballesteros, J. A., Santibáñez‐López, C. E., Baker, C. M., Benavides, L. R., Cunha, T. J., Gainett, G., Ontano, A. Z., Setton, E. V. W., Arango, C. P., Gavish‐Regev, E., et al. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac021 · Cited by 110 · see citing works
Annelid functional genomics reveal the origins of bilaterian life cycles
Bump, P. A., Liang, Y., Guynes, K., Carrillo‐Baltodano, A. M., Davies, B. E., Donnellan, R. D., Tan, Y., Moggioli, G., Seudre, O., Tran, M., et al. (2023) · Nature · doi:10.1038/s41586-022-05636-7 · Cited by 109 · see citing works
Self-citationLack of support for Deuterostomia prompts reinterpretation of the first Bilateria
Kapli, P., Natsidis, P., Leite, D. J., Fursman, M., Jeffrie, N., Rahman, I. A., Philippe, H., Copley, R. R., & Telford, M. J. (2021) · Science Advances · doi:10.1126/sciadv.abe2741 · Cited by 100 · see citing works
Conservative route to genome compaction in a miniature annelid
Martín-Durán, J. M., Vellutini, B. C., Marlétaz, F., Cetrangolo, V., Cvetešić, N., Thiel, D. J., Henriet, S., Grau‐Bové, X., Carrillo‐Baltodano, A. M., Gu, W., et al. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-01327-6 · Cited by 91 · see citing works
Self-citationMulti‐level convergence of complex traits and the evolution of bioluminescence
Lau, E. S., & Oakley, T. H. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12672 · Cited by 90 · see citing works
Ontano, A. Z., Gainett, G., Aharon, S., Ballesteros, J. A., Benavides, L. R., Corbett, K. F., Gavish‐Regev, E., Harvey, M. S., Monsma, S. A., Santibáñez‐López, C. E., et al. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab038 · Cited by 89 · see citing works
The Nereid on the rise: Platynereis as a model system
Özpolat, B. D., Randel, N., Williams, E. A., Bezares-Calderón, L. A., Andreatta, G., Balavoine, G., Bertucci, P. Y., Ferrier, D. E. K., Gambi, M. C., Gazave, E., et al. (2021) · EvoDevo · doi:10.1186/s13227-021-00180-3 · Cited by 85 · see citing works
The little skate genome and the evolutionary emergence of wing-like fins
Marlétaz, F., de la Calle-Mustienes, E., Acemel, R. D., Paliou, C., Naranjo, S., Martínez-García, P. M., Cases, I., Sleight, V. A., Hirschberger, C., Marcet-Houben, M., et al. (2023) · Nature · doi:10.1038/s41586-023-05868-1 · Cited by 71 · see citing works
Self-citationDiversity of cilia-based mechanosensory systems and their functions in marine animal behaviour
Bezares-Calderón, L. A., Berger, J., & Jékely, G. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0376 · Cited by 81 · see citing works
Schwaha, T., Ostrovsky, A. N., & Wanninger, A. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12583 · Cited by 81 · see citing works
A genome-based phylogeny for Mollusca is concordant with fossils and morphology
Chen, Z., Baeza, J. A., Chen, C., González, M. T., González, V. L., Greve, C., Kocot, K. M., Arbizu, P. M., Moles, J., Schell, T., et al. (2025) · Science · doi:10.1126/science.ads0215 · Cited by 69 · see citing works
Neuronal coordination of motile cilia in locomotion and feeding
Marinković, M., Berger, J., & Jékely, G. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0165 · Cited by 67 · see citing works
Lücking, R. (2019) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2019.1650517 · Cited by 67 · see citing works
Beyond Casual Resemblance: Rigorous Frameworks for Comparing Regeneration Across Species
Srivastava, M. (2021) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120319-114716 · Cited by 66 · see citing works
Dicyemida and Orthonectida: Two Stories of Body Plan Simplification
Zverkov, O. A., Mikhailov, K. V., Isaev, S. V., Rusin, L. Y., Popova, O. V., Logacheva, M. D., Penin, A. A., Moroz, L. L., Panchin, Y. V., Lyubetsky, V., et al. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00443 · Cited by 65 · see citing works
Arthropod Origins: Integrating Paleontological and Molecular Evidence
Edgecombe, G. D. (2020) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-011720-124437 · Cited by 65 · see citing works
Early embryogenesis and organogenesis in the annelid Owenia fusiformis
Carrillo‐Baltodano, A. M., Seudre, O., Guynes, K., & Martín-Durán, J. M. (2021) · EvoDevo · doi:10.1186/s13227-021-00176-z · Cited by 64 · see citing works
Animal origins: The record from organic microfossils
Slater, B. J., & Bohlin, M. S. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.104107 · Cited by 61 · see citing works
Dorsoventral decoupling of Hox gene expression underpins the diversification of molluscs
Huan, P., Wang, Q., Tan, S., & Liu, B. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907328117 · Cited by 58 · see citing works
Capela, R., Garric, J., Castro, L. F., & Santos, M. (2019) · Science of the Total Environment · doi:10.1016/j.scitotenv.2019.135740 · Cited by 37 · see citing works
Martínez, A., Bonaglia, S., Domênico, M. D., Fonseca, G., Ingels, J., Jörger, K. M., Laumer, C., Leasi, F., Zeppilli, D., Baldrighi, E., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-07888-1 · Cited by 54 · see citing works
Budd, G. E., & Mann, R. P. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0110 · Cited by 54 · see citing works
Hernandez, A. M., & Ryan, J. F. (2019) · doi:10.1101/729103 · Cited by 52 · see citing works
Recent progress in reconstructing lophotrochozoan (spiralian) phylogeny
Bleidorn, C. (2019) · Organisms Diversity & Evolution · doi:10.1007/s13127-019-00412-4 · Cited by 51 · see citing works
An Emerging Frontier in Intercellular Communication: Extracellular Vesicles in Regeneration
Avalos, P. N., & Forsthoefel, D. J. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.849905 · Cited by 49 · see citing works
Beckers, P., Helm, C., & Bartolomaeus, T. (2019) · BMC Evolutionary Biology · doi:10.1186/s12862-019-1498-9 · Cited by 49 · see citing works
Natsidis, P., Schiffer, P. H., Salvador‐Martínez, I., & Telford, M. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-55573-1 · Cited by 49 · see citing works
Martín-Durán, J. M., & Marlétaz, F. (2020) · Development · doi:10.1242/dev.181081 · Cited by 48 · see citing works
Self-citationScaphopoda is the sister taxon to Bivalvia: Evidence of ancient incomplete lineage sorting
Song, H., Wang, Y., Shao, H., Li, Z., Hu, P., Yap-Chiongco, M. K., Shi, P., Zhang, T., Li, C., Wang, Y., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2302361120 · Cited by 46 · see citing works
Fleas are parasitic scorpionflies
Tihelka, E., Giacomelli, M., Huang, D., Pisani, D., Donoghue, P. C. J., & Cai, C. (2020) · Palaeoentomology · doi:10.11646/palaeoentomology.3.6.16 · Cited by 43 · see citing works
Nemertean, Brachiopod, and Phoronid Neuropeptidomics Reveals Ancestral Spiralian Signaling Systems
Thiel, D. J., Yáñez-Guerra, L. A., Franz‐Wachtel, M., Hejnol, A., & Jékely, G. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab211 · Cited by 42 · see citing works
Evolution and development of complex eyes: a celebration of diversity
Koenig, K. M., & Gross, J. M. (2020) · Development · doi:10.1242/dev.182923 · Cited by 41 · see citing works
Systematic errors in orthology inference and their effects on evolutionary analyses
Natsidis, P., Kapli, P., Schiffer, P. H., & Telford, M. J. (2021) · iScience · doi:10.1016/j.isci.2021.102110 · Cited by 41 · see citing works
Identifying and addressing methodological incongruence in phylogenomics: A review
Fleming, J. F., Valero‐Gracia, A., & Struck, T. H. (2023) · Evolutionary Applications · doi:10.1111/eva.13565 · Cited by 39 · see citing works
Juravel, K., Porras, L., Höhna, S., Pisani, D., & Wörheide, G. (2023) · PLoS ONE · doi:10.1371/journal.pone.0282444 · Cited by 38 · see citing works
Nanglu, K., Cole, S. R., Wright, D. F., & Souto, C. (2022) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12908 · Cited by 37 · see citing works
Canadia spinosa and the early evolution of the annelid nervous system
Parry, L. A., & Caron, J. (2019) · Science Advances · doi:10.1126/sciadv.aax5858 · Cited by 37 · see citing works
Relative Model Fit Does Not Predict Topological Accuracy in Single-Gene Protein Phylogenetics
Spielman, S. J. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa075 · Cited by 37 · see citing works
DNA Sequences Are as Useful as Protein Sequences for Inferring Deep Phylogenies
Kapli, P., Kotari, I., Telford, M. J., Goldman, N., & Yang, Z. (2023) · Systematic Biology · doi:10.1093/sysbio/syad036 · Cited by 36 · see citing works
Li, Y., Nong, W., Baril, T., Yip, H. Y., Swale, T., Hayward, A., Ferrier, D. E. K., & Hui, J. H. L. (2020) · BMC Genomics · doi:10.1186/s12864-020-07027-6 · Cited by 36 · see citing works
Ediacaran metazoan reveals lophotrochozoan affinity and deepens root of Cambrian Explosion
Shore, A., Wood, R. A., Butler, I. B., Zhuravlev, A. Y., McMahon, S., Curtis, A., & Bowyer, F. T. (2021) · Science Advances · doi:10.1126/sciadv.abf2933 · Cited by 34 · see citing works
Sharma, P. P., Ballesteros, J. A., & Santibáñez‐López, C. E. (2021) · Diversity · doi:10.3390/d13110568 · Cited by 33 · see citing works
ERK1/2 is an ancestral organising signal in spiral cleavage
Seudre, O., Carrillo‐Baltodano, A. M., Liang, Y., & Martín-Durán, J. M. (2022) · Nature Communications · doi:10.1038/s41467-022-30004-4 · Cited by 32 · see citing works
Hox gene expression during development of the phoronid Phoronopsis harmeri
Gąsiorowski, L., & Hejnol, A. (2020) · EvoDevo · doi:10.1186/s13227-020-0148-z · Cited by 31 · see citing works
Ancestral Role of Ecdysis-Related Neuropeptides in Animal Life Cycle Transitions
Zieger, E., Robert, N. S. M., Calcino, A., & Wanninger, A. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.004 · Cited by 31 · see citing works
Tan, S., Huan, P., & Liu, B. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab322 · Cited by 30 · see citing works
Yu, D., Ding, Y., Tihelka, E., Cai, C., Hu, F., Liu, M., & Zhang, F. (2022) · Systematic Biology · doi:10.1093/sysbio/syac024 · Cited by 30 · see citing works
Zhang, L., He, J. G., Tan, P., Gong, Z., Qian, S., Miao, Y., Zhang, H., Tu, G., Chen, Q., Zhong, Q., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03176-4 · Cited by 30 · see citing works
Polyzoa is back: The effect of complete gene sets on the placement of Ectoprocta and Entoprocta
Khalturin, K., Shunatova, N., Shchenkov, S. V., Sasakura, Y., Kawamitsu, M., & Satoh, N. (2022) · Science Advances · doi:10.1126/sciadv.abo4400 · Cited by 30 · see citing works
Self-citationThe complex evolutionary history of sulfoxide synthase in ovothiol biosynthesis
Gerdol, M., Sollitto, M., Pallavicini, A., & Castellano, I. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1812 · Cited by 30 · see citing works
Andrikou, C., Passamaneck, Y. J., Lowe, C. J., Martindale, M. Q., & Hejnol, A. (2019) · EvoDevo · doi:10.1186/s13227-019-0146-1 · Cited by 28 · see citing works
A Cambrian tommotiid preserving soft tissues reveals the metameric ancestry of lophophorates
Guo, J. C., Parry, L. A., Vinther, J., Edgecombe, G. D., Wei, F., Zhao, J., Zhao, Y., Béthoux, O., Lei, X., Chen, A., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.09.011 · Cited by 28 · see citing works
The evolution of the metazoan Toll receptor family and its expression during protostome development
Orús-Alcalde, A., Lu, T.-M., Børve, A., & Hejnol, A. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-021-01927-1 · Cited by 27 · see citing works
Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies
Ross, L., Mongue, A. J., Hodson, C. N., & Schwander, T. (2022) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-021822-010659 · Cited by 27 · see citing works
Seudre, O., Martín-Zamora, F. M., Rapisarda, V., Luqman, I., Carrillo‐Baltodano, A. M., & Martín-Durán, J. M. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac139 · Cited by 27 · see citing works
Mulhair, P. O., McCarthy, C. G. P., Siu-Ting, K., Creevey, C. J., & O’Connell, M. J. (2022) · Current Biology · doi:10.1016/j.cub.2022.10.036 · Cited by 27 · see citing works
Martynov, A. V., Lundin, K., PICTON, B. E., Fletcher, K. C., Malmberg, K., & Korshunova, T. (2020) · PLoS ONE · doi:10.1371/journal.pone.0227173 · Cited by 27 · see citing works
Drábková, M., Kocot, K. M., Halanych, K. M., Oakley, T. H., Moroz, L. L., Cannon, J. T., Kuris, A. M., Garcia‐Vedrenne, A. E., Pankey, M. S., Ellis, E. A., et al. (2022) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2022.0683 · Cited by 26 · see citing works
Ancestral morphology of Ecdysozoa constrained by an early Cambrian stem group ecdysozoan
Howard, R. J., Edgecombe, G. D., Shi, X., Hou, X., & Ma, X. (2020) · BMC Evolutionary Biology · doi:10.1186/s12862-020-01720-6 · Cited by 26 · see citing works
Structural and evolutionary insights into astacin metallopeptidases
Gomis‐Rüth, F. X., & Stöcker, W. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1080836 · Cited by 26 · see citing works
Embryonic development in the acoel Hofstenia miamia
Kimura, J. O., Ricci, L., & Srivastava, M. (2021) · Development · doi:10.1242/dev.188656 · Cited by 25 · see citing works
Late Ediacaran organic microfossils from Finland
Willman, S., & Slater, B. J. (2021) · Geological Magazine · doi:10.1017/s0016756821000753 · Cited by 25 · see citing works
Amiskwia is a large Cambrian gnathiferan with complex gnathostomulid-like jaws
Caron, J., & Cheung, B. (2019) · Communications Biology · doi:10.1038/s42003-019-0388-4 · Cited by 24 · see citing works
The early animal radiation: insights from interpreting the Cambrian problematic fossils
Cong, P. (2023) · Frontiers in Earth Science · doi:10.3389/feart.2023.1120118 · Cited by 23 · see citing works
Fossil Constraints on the Timescale of Parasitic Helminth Evolution
Baets, K. D., Dentzien‐Dias, P., Harrison, G. W. M., Littlewood, D. T. J., & Parry, L. A. (2021) · Topics in geobiology · doi:10.1007/978-3-030-42484-8_7 · Cited by 23 · see citing works
Fusion, fission, and scrambling of the bilaterian genome in BryozoaPreprint
Lewin, T. D., Liao, I. J.-Y., Chen, M.-E., Bishop, J., Holland, P. W. H., & Luo, Y. (2025) · Genome Research · doi:10.1101/gr.279636.124 · Cited by 23 · see citing works
Roberts, N. G., Gilmore, M. J., Struck, T. H., & Kocot, K. M. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae254 · Cited by 22 · see citing works
Brachionus rotifers as a model for investigating dietary and metabolic regulators of aging
Gribble, K. E. (2020) · Nutrition and Healthy Aging · doi:10.3233/nha-200104 · Cited by 22 · see citing works
Transitional chordates and vertebrate origins: Tunicates
Fodor, A., Liu, J., Turner, L., & Swalla, B. J. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.10.001 · Cited by 22 · see citing works
Zou, S., & Pan, B. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00829-z · Cited by 22 · see citing works
Herlyn, H. (2021) · Topics in geobiology · doi:10.1007/978-3-030-42484-8_8 · Cited by 22 · see citing works
Gąsiorowski, L., Børve, A., Cherneva, I. A., Orús-Alcalde, A., & Hejnol, A. (2021) · BMC Biology · doi:10.1186/s12915-021-01113-1 · Cited by 21 · see citing works
Spiralian genomics and the evolution of animal genome architecture
Liao, I. J.-Y., Lu, T.-M., Chen, M.-E., & Luo, Y. (2023) · Briefings in Functional Genomics · doi:10.1093/bfgp/elad029 · Cited by 21 · see citing works
Genes with spiralian-specific protein motifs are expressed in spiralian ciliary bands
Wu, L., Hiebert, L. S., Klann, M., Passamaneck, Y. J., Bastin, B. R., Schneider, S., Martindale, M. Q., Seaver, E. C., Maslakova, S. A., & Lambert, J. D. (2020) · Nature Communications · doi:10.1038/s41467-020-17780-7 · Cited by 21 · see citing works
Is the deuterostome clade an artifact?
Silva, A. S., Natsidis, P., Piovani, L., Kapli, P., & Telford, M. J. (2025) · Current Biology · doi:10.1016/j.cub.2025.06.045 · Cited by 20 · see citing works
Phoronid genome supports a monophyletic Lophophorata.
Lewin, T. D., Sakagami, T., Kao, L.-J., Liao, I. J.-Y., Chiu, Y.-L., Piñón-González, V. M., Li, J.-Y., Tin, K.-X., Lu, M., Endo, K., et al. (2025) · Current Biology · doi:10.1016/j.cub.2025.10.020 · Cited by 15 · see citing works
Bekkouche, N., & Gąsiorowski, L. (2022) · Journal of Systematic Palaeontology · doi:10.1080/14772019.2022.2109217 · Cited by 20 · see citing works
A giant stem-group chaetognath
Park, T. S., Nielsen, M. L., Parry, L. A., Sørensen, M. V., Lee, M., Kihm, J., Ahn, I., Park, C., Vivo, G. D., Smith, M. P., et al. (2024) · Science Advances · doi:10.1126/sciadv.adi6678 · Cited by 20 · see citing works
Ge, X., Peng, L., Morse, J. C., Wang, J., Zang, H., Yang, L., ChangHai, S., & Wang, B. (2024) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2024.108196 · Cited by 20 · see citing works
Guynes, K., Sarre, L. A., Carrillo‐Baltodano, A. M., Davies, B. E., Xu, L., Liang, Y., Martín-Zamora, F. M., Hurd, P. J., de Mendoza, A., & Martín-Durán, J. M. (2024) · Genome biology · doi:10.1186/s13059-024-03346-z · Cited by 19 · see citing works
Daily rhythms in gene expression of the human parasite Schistosoma mansoni
Rawlinson, K. A., Reid, A. J., Lu, Z., Driguez, P., Wawer, A., Coghlan, A., Sankaranarayanan, G., Buddenborg, S. K., Soria, C. D., McCarthy, C. A., et al. (2021) · BMC Biology · doi:10.1186/s12915-021-01189-9 · Cited by 19 · see citing works
A Cambrian spiny stem mollusk and the deep homology of lophotrochozoan scleritomes
Zhang, G., Parry, L. A., Vinther, J., & Ma, X. (2024) · Science · doi:10.1126/science.ado0059 · Cited by 18 · see citing works
Schuster, H. C., & Hirth, F. (2023) · Science Advances · doi:10.1126/sciadv.ade8259 · Cited by 17 · see citing works
Yu, D., Du, S., Xiping, W. E. I., Jie, Z. H. U., Ding, Y., Hu, F., Liu, M., & Zhang, F. (2024) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2024.108169 · Cited by 17 · see citing works
Cutting the long branches: Consilience as a path to unearth the evolutionary history of Gnetales
Coiro, M., Roberts, E. A., Hofmann, C.-C., & Seyfullah, L. J. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.1082639 · Cited by 16 · see citing works
Evolution of Bilateria from a Meiofauna Perspective—Miniaturization in the Focus
Worsaae, K., Vinther, J., & Sørensen, M. V. (2023) · Springer eBooks · doi:10.1007/978-3-031-21622-0_1 · Cited by 16 · see citing works
- Authors
- Marlétaz, F., Peijnenburg, K. T. C. A., Goto, T., Satoh, N., & Rokhsar, D. S.
- Affiliations
- Okinawa Institute of Science and Technology Graduate University (JP)
- Naturalis Biodiversity Center (NL)
- Mie University (JP)
- Corresponding author
- Marlétaz, Ferdinand
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 29
- Issue
- 2
- Pages
- 312-318.e3
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2908647854
- Cited by
- 268
- References
- 50
- Citations by year
- 2026: 24 · 2025: 33 · 2024: 28 · 2023: 34 · 2022: 30 · 2021: 45 · 2020: 41 · 2019: 32
- FWCI
- 29.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
- Okinawa Institute of Science and Technology Graduate University (Okinawa Institute of Science and Technology Graduate University) (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Okinawa Institute of Science and Technology Graduate University
- European Research Council (268513)
- Netherlands Organization for Scientific Research (863.08.024, 016.161.351)
- NSF (OCE-1029478, OCE-1338959)
- UK NERC
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- chaetognaths, Gnathifera, Lophotrochozoa, phylogenomics, transcriptome, rotifers, Lophophorata, secondary losses, bilaterian evolution, compositional heterogeneity
- MeSH terms
- Animals, Invertebrates, Phylogeny, Evolution, Molecular, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
