A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals.
Resolving the early diversification of animal lineages has proven difficult, even using genome-scale datasets. Several phylogenomic studies have supported the classical scenario in which sponges (Porifera) are the sister group to all other animals ("Porifera-sister" hypothesis), consistent with a single origin of the gut, nerve cells, and muscle cells in the stem lineage of eumetazoans (bilaterians + ctenophores + cnidarians). In contrast, several other studies have recovered an alternative topology in which ctenophores are the sister group to all other animals (including sponges). The "Ctenophora-sister" hypothesis implies that eumetazoan-specific traits, such as neurons and muscle cells, either evolved once along the metazoan stem lineage and were then lost in sponges and placozoans or evolved at least twice independently in Ctenophora and in Cnidaria + Bilateria. Here, we report on our reconstruction of deep metazoan relationships using a 1,719-gene dataset with dense taxonomic sampling of non-bilaterian animals that was assembled using a semi-automated procedure, designed to reduce known error sources. Our dataset outperforms previous metazoan gene superalignments in terms of data quality and quantity. Analyses with a best-fitting site-heterogeneous evolutionary model provide strong statistical support for placing sponges as the sister-group to all other metazoans, with ctenophores emerging as the second-earliest branching animal lineage. Only those methodological settings that exacerbated long-branch attraction artifacts yielded Ctenophora-sister. These results show that methodological issues must be carefully addressed to tackle difficult phylogenetic questions and pave the road to a better understanding of how fundamental features of animal body plans have emerged.
Sorbonne Universités, UPMC Univ Paris 06, CNRS, Evolution Paris-Seine UMR7138, Institut de Biologie Paris-Seine, Case 05, 7 quai St Bernard, 75005 Paris, France.
Paul
P
Simion
Centre de Théorisation et de Modélisation de la Biodiversité, Station d'Ecologie Théorique et Expérimentale, UMR CNRS 5321, Moulis 09200, France; Département de Biochimie, Centre Robert-Cedergren, Université de Montréal, Montréal, QC H3C 3J7, Canada. Electronic address: herve.philippe@sete.cnrs.fr.
Hervé
H
Philippe
InBios-Eukaryotic Phylogenomics, Department of Life Sciences and PhytoSYSTEMS, University of Liège, Bât. B22, Quartier Vallée 1, Chemin de la Vallée 4, 4000 Liège, Belgium.
Denis
D
Baurain
Sorbonne Universités, UPMC Univ Paris 06, CNRS, Evolution Paris-Seine UMR7138, Institut de Biologie Paris-Seine, Case 05, 7 quai St Bernard, 75005 Paris, France.
Muriel
M
Jager
Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200, USA; CNRS, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France; Sorbonne Universités, Université Pierre et Marie Curie (UPMC) Paris 06, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France.
Daniel J
DJ
Richter
Centre de Théorisation et de Modélisation de la Biodiversité, Station d'Ecologie Théorique et Expérimentale, UMR CNRS 5321, Moulis 09200, France.
Arnaud
A
Di Franco
Centre de Théorisation et de Modélisation de la Biodiversité, Station d'Ecologie Théorique et Expérimentale, UMR CNRS 5321, Moulis 09200, France; Département de Biochimie, Centre Robert-Cedergren, Université de Montréal, Montréal, QC H3C 3J7, Canada.
Béatrice
B
Roure
Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
Nori
N
Satoh
Sorbonne Universités, UPMC Univ Paris 06, CNRS, Evolution Paris-Seine UMR7138, Institut de Biologie Paris-Seine, Case 05, 7 quai St Bernard, 75005 Paris, France.
Éric
É
Quéinnec
Aix Marseille Univ, Univ Avignon, CNRS, IRD, IMBE, Marseille, France, Chemin de la Batterie des Lions, 13007 Marseille, France; Department of Embryology, Faculty of Biology, Saint-Petersburg State University, Universitetskaya nab. 7/9, Saint-Petersburg 199034, Russia.
Alexander
A
Ereskovsky
Sorbonne Universités, UPMC Univ Paris 06, and CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer, Observatoire Océanographique, 06230 Villefranche-sur-mer, France.
Pascal
P
Lapébie
CNRS, FR2424, ABiMS, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France; Sorbonne Universités, Université Pierre et Marie Curie (UPMC) Paris 06, FR2424, ABiMS, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France.
Erwan
E
Corre
Université de Montpellier (UM), Institut des Sciences de l'Évolution (ISEM), UMR 5554 CNRS-IRD-EPHE, Case Courier 64, Place Eugène Bataillon, 34095 Montpellier, France.
Frédéric
F
Delsuc
Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200, USA.
Nicole
N
King
Department of Earth and Environmental Sciences & GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333 München, Germany; SNSB - Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Str. 10, 80333 München, Germany.
Gert
G
Wörheide
Sorbonne Universités, UPMC Univ Paris 06, CNRS, Evolution Paris-Seine UMR7138, Institut de Biologie Paris-Seine, Case 05, 7 quai St Bernard, 75005 Paris, France. Electronic address: michael.manuel@upmc.fr.
Michaël
M
Manuel
D000818:Animals; D005075:Biological Evolution; D016678:Genome; D023281:Genomics / Q000379:methods; D007448:Invertebrates / Q000145:classification* / Q000235:genetics; D010802:Phylogeny; D011161:Porifera / Q000145:classification / Q000235:genetics*; D014714:Vertebrates / Q000145:classification* / Q000235:genetics
Ctenophora; Eumetazoa; Porifera; animal; evolution; long branch attraction; metazoa; nervous system; phylogenomics; phylogeny