Genomic data do not support comb jellies as the sister group to all other animals
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.
© 2015 National Academy of Sciences. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved November 2, 2015 (received for review September 11, 2015). Published ahead of print November 30, 2015. We are indebted to the computational resources at the University of Bristol and the Iowa State University High Performance Computing Group. We thank the Leibniz Supercomputing Centre of the Bavarian Academy of Sciences and Humanities for the provisioning and support of Cloud computing infrastructure essential to this publication. René Neumeier is highly acknowledged for setting up and maintaining computational resources at Ludwig-Maximilians-Universität München Geobiology. We thank the associate editor and two anonymous reviewers for their constructive comments. We are also indebted to Prof. Eric Davidson for his help and encouragement while composing the manuscript. G.W. was funded by the German Research Foundation [Deutsche Forschungsgemeinschaft (DFG)] and the Ludwig-Maximilians-Universität München LMUexcellent program (Project MODELSPONGE) through the German Excellence Initiative. M.D. was funded through DFG Grants DO 1742/1-1,2. W.P. and N.L. were funded by the Agence Nationale de la Recherche (ANR) grant Ancestrome ANR-10-BINF-01-01. 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. Freely available online through the PNAS open access option. 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.
Published - PNAS-2015-Pisani-15402-7.pdf
Supplemental Material - pnas.201518127SI.pdf