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

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 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...

Miscues misplace sponges

“…In contrast to several recent publications (1-5), Pisani et al (6) claim that (i) genomic data do not support ctenophores as the sister group to other animals and (ii) independent evolution of complex features (e.g., neurons, muscles) in ctenophores is not supported. These claims are based on selective interpretation, subjective criteria, and improper assumptions about original analyses.…”

“…For example, the Whelan-16 dataset modeled 89 data partitions, not 1, as implied by Pisani et al (6). Thus, claims from model validation tests are unsupported because approaches used by others (1, 2) were not examined.…”

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…S14), where the bacterial stem was predicted to have experienced 4.79 substitutions per site, compared with a mean of 0.192 (range, 0.0157-0.546) for within-domain branches. The use of long outgroup branches is a general problem that has contributed to disagreements about the archaeal root as well as about the roots of other major radiations (58)(59)(60)(61), motivating a search for alternative rooting methods.…”

Ediacaran developmental biology

“…The presence of discrete (as opposed to diffuse) growth tips would argue against affinities with most members of Rouphozoa and Gnathifera, but the likely presence of multiple axial growth zones (in Charnia ) and potential secondary growth tips (in Bradgatia ), is reconcilable with known variation in members of the colonial cnidarians. Based on current data, we cannot rule out a stem‐metazoan affinity for rangeomorphs (if Porifera are the sister lineage to all other metazoans; Pisani et al , 2015), or, indeed, a stem‐poriferan affinity, but the general paucity, as opposed to conflict, of data prevents further assessment (Fig. 7).…”