Ctenophora is not a sister group to other animals after all

Since 2008 there have been a debate whether the phylum Ctenophora is a phylogenetic sister group to other animals or not (Dunn et al. 2008; Philippe et al. 2009). There were some who claimed to have resolved the debate (that Ctenophora really is a sister group to other animals: Ryan et al. 2013), but the presented evidence was not at all convincing, as I discussed some time ago. Recently, another paper (Whelan et al. 2015) came out that favoured Ctenophora as the sister group to other animals (hereafter referred to as Ctenophora-basal tree), but this time the results were much more convincing and I was prepared to believe the Ctenophora-basal tree.

But not so fast. It turns out I was fooled. Only half a year after the Whelan et al. (2015) publication, Pisani et al. (2015) showed that the analyses by Whelan et al., as well as all previous analyses favouring Ctenophora-basal tree, were still plagued by systematic errors. Pisani et al. (2015) found that the sponges (Porifera) are probably the sister group to other animals (as is usually assumed) after all, although exact position of Ctenophora relative to the remaining animals still needs additional research. For me, one of the most striking results from Pisani et al. (2015) was the re-analysis of genome content data (presence/absence of protein coding genes) from Ryan et al. (2013). The genome content tree that Ryan et al. (2013) recovered, contained several phylogenetic relationships that are highly suspect (e.g. non-monophyly of Annelida and a group containing a mollusc, an annelid and a chordate Branchiostoma). Remarkably, when Pisani et al. (2015) used a less biased model of gene content evolution, which does not underestimate gene losses as much as did the model used by Ryan et al. (2013), they recovered an animal tree of life that fully agreed with independent phylogenomic analyses based gene sequences. There was not a single nonsense clade left. And in that tree, Porifera replaced Ctenophora as the sister group to other animals.

As for the Whelan et al. (2015) study that fooled me, the main issue comes down to the choice of an out-group. Whelan et al. (2015) analysed some of their datasets also with more realistic, but computationally more demanding CAT model, but recovered nevertheless Ctenophora-basal tree. It turns out, though, that when more distant out-groups to animals (Fungi or Fungi plus non-choanoflagllate members of Holozoa) are excluded from the analysis (retaining only the members of Holozoa or only the choanoflagllates), Whelan et al. (2015) datasets do not support Ctenophora-basal tree anymore or even favour Porifera-basal tree. Whelan et al. (2015) actually did analyse their datasets also with alternative out-group compositions, but only with simpler evolutionary models and therefore it was not possible to discover that different out-group compositions affect results when using more complex CAT model! Such a simple trick which the authors could have done to test their results...

Another recent study also found Ctenophora-basal tree (Chang et al. 2015) using the CAT model. Although Chang et al. (2015) analyses did not include Fungi, it was not tested if excluding more distant non-choanoflagllate Holozoa taxa could affect the results. But this Ctenophora question was not the topic of this paper (it was about Myxozoa, highly reduced parasitic Cnidaria), although one of the co-authors was (Hervé Philippe) also a co-author in Pisani et al. (2015) paper, which studied the effect of out-group composition.

Still, it is disconcerting that depending on the composition of the out-group, even if the closest relatives are included, the results can change that dramatically: using CAT model and including Fungi, the Ctenophora-basal tree can be recovered with maximal statistical support, but using CAT model and excluding all out-groups except choanoflagllates (the closest relatives of animals), Porifera-basal tree can be recovered with maximal support instead. I would have thought that as long as the closest out-groups are also included (choanoflagllates) in the analyses, the more distant out-groups (Fungi) should not influence the results that much. This tells me again (as I discussed before) that whatever phylogenetic signal there is for the relationships between Porifera, Ctenophora, Placozoa, Cnidaria, and Bilateria, it is quite tiny. These groups separated from each other in the Precambrian (>540 Ma) probably rather rapidly, perhaps within a few tens of millions of years or even within a shorter time period. Because it starts to look like the nervous systems and perhaps muscles might have evolved independently even three times in Ctenophora, Cnidaria, and Bilateria (Liebeskind et al. 2015; Moroz et al. 2014), it seems to be of less importance what are the exact phylogenetic relationships between Porifera, Ctenophora, Placozoa, Cnidaria, and Bilateria. Ctenophora, Cnidaria, and Bilateria might have evolved their morphological complexity independently from Porifera or Placozoa-like ancestors.


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