Deep metazoan phylogeny: When different genes tell different stories

Nosenko, Tetyana; Schreiber, Franziska; Adamska, Maja; Adamski, Marcin; Eitel, Michael; Hammel, Jörg U.; Maldonado, Manuel; Müller, Wernér E.G.; Nickel, Michael; Schierwater, Bernd; Vacelet, Jean; Wiens, Matthias; Wörheide, Gert

doi:10.1016/j.ympev.2013.01.010

Cited by 241 publications

(246 citation statements)

References 78 publications

Supporting

Mentioning

224

Contrasting

Unclassified

Order By: Relevance

“…We investigated whether previous studies supporting Ctenophora-sister were conducted using adequately fitting substitution models. Using three exemplar datasets, which we call Ryan-Choano, Moroz-3D, and Whelan-6-Choano (details are provided below and in Methods), we compared the relative fit of site-homogeneous and siteheterogeneous models using Bayesian cross-validation (36, 37), a routine statistical technique used to evaluate the predictive performance of a probabilistic model, which has been commonly used in the context of phylogenetics (23,24,(38)(39)(40)(41). Using 10 cross-validation replicates, we found that in all cases, site-heterogeneous models fit these data significantly better than the site-homogeneous models that previous studies mostly relied upon ( Table 1).…”

Section: Resultsmentioning

confidence: 99%

“…To address this issue, site-heterogeneous models have been developed (22), which relax the homogeneity assumption to account for site-specific biochemical constraints. Although computationally more demanding, their increased capacity to identify convergent evolution is reflected in the better statistical fit these models generally provide to many empirical datasets (e.g., 23,24). Here, we used a common statistical technique, Bayesian cross-validation, to compare the fit of site-homogeneous and site-heterogeneous models, and investigate whether previous studies that recovered Ctenophora-sister were influenced by the use of poorly fitting substitution models.…”

Section: Addressing Biases In Phylogenetic Reconstructionmentioning

confidence: 99%

See 1 more Smart Citation

Genomic data do not support comb jellies as the sister group to all other animals

Pisani

Pett

Dohrmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

300

336

View full text Add to dashboard Cite

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 R esolving the phylogenetic relationships close to the root of the animal tree of life, which encompass the phyla Porifera (sponges), Cnidaria (jellyfish, corals, and their allies), Ctenophora (comb jellies), Placozoa (the "plate animals" of the genus Trichoplax), and Bilateria (the group containing all remaining phyla), is fundamental to understanding early animal evolution and the emergence of complex traits [reviewed by Dohrmann and Wörheide (1)]. Traditionally, sponges have been recognized as the sister group to the remaining animals (the "Porifera-sister" hypothesis). Under this scenario, true epithelia (with belt desmosomes connecting neighboring cells) and extracellular digestion are conventionally thought to have been primitively absent in sponges, having evolved in the common ancestor of Placozoa, Ctenophora, Cnidaria, and Bilateria. Within this group, gap junctions between neighboring cells, ectodermal and endodermal germ layers, sensory cells, nerve cells, and muscle cells evolved only once in the common ancestor of Ctenophora, Cnidaria, and Bilateria. Thus, Porifera-sister is consistent with the view that the last common ancestor of the animals was relatively simple and more complex body plans evolved after sponges had separated from the other animal lineages. However, a s...

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Addressing Biases In Phylogenetic Reconstructionmentioning

confidence: 99%

Genomic data do not support comb jellies as the sister group to all other animals

Pisani

Pett

Dohrmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

300

336

View full text Add to dashboard Cite

show abstract

“…Nextgeneration sequencing (NGS) now enables us to generate large data sets for many species at a relatively low cost. The systematic community has necessarily progressed from candidate genes through EST-based methods to 454 and Illumina-based transcriptome and genome datasets to resolve major relationships among the animal phyla (e.g., Dunn et al, 2008;Hejnol et al, 2009;Nosenko et al, 2013;Ryan et al, 2013;Moroz et al, 2014). Long outstanding issues have been resolved for within-phylum relationships among arthropods, molluscs, and annelids, to mention just some of the largest animal phyla (e.g., Meusemann et al, 2010;Kocot et al, 2011;Smith et al, 2011;Struck et al, 2011;von Reumont et al, 2012;Andrade et al, 2014;Weigert et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Re-evaluating the phylogeny of Sipuncula through transcriptomics

Lemer

Kawauchi

Andrade

et al. 2015

Molecular Phylogenetics and Evolution

View full text Add to dashboard Cite

“…The final alignments included a high number of ribosomal genes, which were discarded in previous analyses (Dunn et al 2008); ribosomal datasets have been shown to be problematic to infer phylogenies (Nosenko et al 2013). The nuclear-coding gene datasets were analysed using Bayesian inference, but instead of providing posterior probability values, the statistical support was assessed using a nonconventional approach: 100 bootstrap pseudo-replicates were produced and independently analysed with Phylobayes; then, the resulting trees were used to compute the bootstrap support values.…”

Section: A Contrasting Hypothesis: Acoelomorphs Are Deuterostomesmentioning

confidence: 99%

Acoelomorpha: earliest branching bilaterians or deuterostomes?

Ruiz‐Trillo

Paps

2015

Org Divers Evol

View full text Add to dashboard Cite

The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this longstanding issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life.

show abstract

Deep metazoan phylogeny: When different genes tell different stories

Cited by 241 publications

References 78 publications

Genomic data do not support comb jellies as the sister group to all other animals

Genomic data do not support comb jellies as the sister group to all other animals

Re-evaluating the phylogeny of Sipuncula through transcriptomics

Acoelomorpha: earliest branching bilaterians or deuterostomes?

Contact Info

Product

Resources

About