Genomic data do not support comb jellies as the sister group to all other animals
Davide Pisani a,b,1, Walker Pett c, Martin Dohrmann d, Roberto Feuda e, Omar Rota-Stabelli f, Hervé Philippe g,h, Nicolas Lartillot c, and Gert Wörheide d,i,1
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TG, United Kingdom;
bSchool of Biological Sciences, University of Bristol, Bristol BS8 1TG, United Kingdom;
cLaboratoire de Biométrie et Biologie Évolutive, Université Lyon 1, CNRS, UMR 5558, 69622 Villeurbanne cedex, France;
dDepartment of Earth & Environmental Sciences & GeoBio-Center, Ludwig-Maximilians-Universität München, Munich 80333, Germany;
eDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125;
fDepartment of Sustainable Agro-Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’ Adige 38010, Italy;
gCentre for Biodiversity Theory and Modelling, USR CNRS 2936, Station d’Ecologie Expérimentale du CNRS, Moulis 09200, France;
hDépartement de Biochimie, Centre Robert-Cedergren, Université de Montréal, Montreal, QC, Canada H3C 3J7;
iBayerische Staatssammlung für Paläontologie und Geologie, Munich 80333, Germany
Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved November 2, 2015 (received for review September 11, 2015)
Sponge - Red Sea - Gert Wörheid
Significance
Clarifying the phylogeny of animals is fundamental to understanding their evolution. Traditionally, sponges have been considered the sister group of all other extant animals, but recent genomic studies have suggested comb jellies occupy that position instead. Here, we analyzed the current genomic evidence from comb jellies and found no convincing support for this hypothesis. Instead, when analyzed with appropriate methods, recent genomic data support the traditional hypothesis. We conclude that the alternative scenario of animal evolution according to which ctenophores evolved morphological complexity independently from cnidarians and bilaterians or, alternatively, sponges secondarily lost a nervous system, muscles, and other characters, is not supported by the available evidence.
Abstract
Understanding how complex traits, such as epithelia, nervous systems, muscles, or guts, originated depends on a well-supported hypothesis about the phylogenetic relationships among major animal lineages. Traditionally, sponges (Porifera) have been interpreted as the sister group to the remaining animals, a hypothesis consistent with the conventional view that the last common animal ancestor was relatively simple and more complex body plans arose later in evolution. However, this premise has recently been challenged by analyses of the genomes of comb jellies (Ctenophora), which, instead, found ctenophores as the sister group to the remaining animals (the “Ctenophora-sister” hypothesis). Because ctenophores are morphologically complex predators with true epithelia, nervous systems, muscles, and guts, this scenario implies these traits were either present in the last common ancestor of all animals and were lost secondarily in sponges and placozoans (Trichoplax) or, alternatively, evolved convergently in comb jellies. Here, we analyze representative datasets from recent studies supporting Ctenophora-sister, including genome-scale alignments of concatenated protein sequences, as well as a genomic gene content dataset. We found no support for Ctenophora-sister and conclude it is an artifact resulting from inadequate methodology, especially the use of simplistic evolutionary models and inappropriate choice of species to root the metazoan tree. Our results reinforce a traditional scenario for the evolution of complexity in animals, and indicate that inferences about the evolution of Metazoa based on the Ctenophora-sister hypothesis are not supported by the currently available data.
Metazoa Ctenophora Porifera phylogenomics evolution
Footnotes
1To whom correspondence may be addressed. Email: davide.pisani{at}bristol.ac.uk or woerheide{at}lmu.de.
Author contributions: D.P. and G.W. designed research; D.P., W.P., and M.D. performed research; W.P., N.L., and G.W. contributed new reagents/analytic tools; D.P., W.P., M.D., R.F., O.R.-S., H.P., N.L., and G.W. analyzed data; D.P., W.P., M.D., R.F., O.R.-S., H.P., N.L., and G.W. wrote the paper; and R.F., O.R.-S., and G.W. created the figures.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The scripts to run our gene content analyses have been deposited in Github, github.com/willpett/ctenophora-gene-content (apart from implementing the methods in MrBayes).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1518127112/-/DCSupplemental.
Freely available online through the PNAS open access option.
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