Why comb jellies complicate animal evolution

By Heiloi Yip

Ctenophores, also known as comb jellies, are a group of jellyfish-like marine organisms found all over the world’s oceans. The complexity of a ctenophore bodyplan is somewhere between that of simple poriferans (sea sponges) and highly complex bilaterians (animals with bilateral symmetry). By intuition, one might draw a phylogenetic tree with the sponges as the basal-most group, followed by the ctenophores and the bilaterians in order of increasing complexity. Indeed, this has been the ‘traditional’ view on the phylogeny of all animals, where the common ancestor was inferred to be a sponge-like multicellular organism. However, modern advances in molecular sequencing have put this phylogenetic tree under question, shaking our fundamental understanding of the evolution of animals.

Firstly, let’s discuss the rationale behind the ‘traditional’ phylogenetic tree. Also known as the ‘Porifera-first’ hypothesis, this tree poses the view that sponges are the basal-most group of animals, as they lack traits that most other animals have. Looking at the morphology of ctenophores reveals that not only do ctenophores possess more advanced traits than sponges, but these traits also happen to be very similar to those seen in cnidarians (true jellyfish). For one, both ctenophores and cnidarians generally appear jellyfish-like, with a round, translucent body and multiple tentacles. Both ctenophores and cnidarians feature traits that sponges lack, such as nerves, muscles and tissue arranged in layers.1,2 In addition, the ctenophore bodyplan also possesses a level of symmetry: while not as complex as bilateral symmetry, their anatomy is still vastly more organized than that of sponges (which have no symmetry at all). Thus, initial attempts at placing ctenophores within the animal phylogenetic tree have often grouped them somewhere close to the cnidarians, making the ctenophores more derived than sponges.2

One problem with determining organism relatedness based on morphology is that it tends to lead to divided opinions, as different paleontologists may interpret the same anatomical trait in different ways. The advent of molecular phylogenetics has provided a more objective way to measure relatedness between organisms, where more related organisms are expected to share a greater proportion of their genomes. But the confusion began when the genomes of ctenophores were sequenced and compared with those of other animals. Paradoxically, the ctenophore genome appears markedly different than other animals, even sponges. With such a unique genome compared to other animals, this genetic dissimilarity would suggest ctenophores are the most basal group of all animals. Thus, despite the complex traits that ctenophores possess, the ‘Ctenophore-first’ hypothesis has quantitative evidence that the ‘Porifera-first’ hypothesis lacked.3

One explanation for this peculiarity is that ctenophores independently evolved all these complex traits. This would be very unlikely, simply because this would involve myriad coincident evolutionary adaptations. It is also possible that the sponges have independently lost these complex traits, though this seems implausible due to the sheer evolutionary advantages such traits would provide.4 A more recent explanation proposes that the ancestral animal may have possessed precursor versions of these traits, such as a very simple nervous system. This would explain how the sponges lost these traits, while the ctenophores and bilaterians independently developed more complex systems. As rational as this explanation sounds, there is insufficient evidence to prove any one theory and disprove the others.5

As if the placement of ctenophores is not confusing enough, there also exists counterevidence against the ‘ctenophore-first’ hypotheses! Meta-analytical reviews of previous phylogenomic analyses report that studies on ctenophore genomes are plagued with systematic errors, particularly at the phylogenetic construction stage. This is by no means the fault of the researchers, rather this has more to do with the highly complicated ctenophore genomes and current limitations in phylogenetic analysis. While the genome of ctenophores may show a big degree of difference compared to other animals, this does not directly indicate that ctenophores are the most ancestral groups – only that the group has experienced the highest rate of evolution. This phenomenon is known as long branch attraction (LBA), and it is suggested that “ctenophore-first” trees are a result of this artefact.6 Current analytical methods have limited ability to discriminate evolution rate and phylogenetic placement, thus resulting in LBA and ctenophores being misplaced as the most basal group. Recent phylogenetic studies that take LBA and other errors into account can reproduce the ‘Porifera-first’ trees under specific circumstances.5,7 Once again, there is supporting evidence (or counter-counterevidence?) for sponges as the single most basal group of animals, followed closely by the ctenophores.

The controversy between the relationship of sponges and ctenophores reflects the conflicts of morphology-based and molecular phylogenies. Both methods have their own unique strengths and weaknesses: no single tree from either method should be taken as the only ‘answer’. As more species get their genomes sequenced and catalogued, molecular phylogenetics are proving to be increasingly relevant due to powerful processing capabilities. However, the prevalence of molecular phylogenetics also augments the need to refine many of the analytical techniques currently employed.

References:

1. Sachkova MY, Nordmann E-L, Soto-Àngel JJ, Meeda Y, Górski B, Naumann B, et al. Neuropeptide repertoire and 3D anatomy of the ctenophore nervous system. Current Biology. 2021 Dec 6;31(23):5274-5285.e6.

2. Jenner RA. Evolution of animal body plans: the role of metazoan phylogeny at the interface between pattern and process. Evolution & Development. 2000;2(4):208–21.

3. Kapli P, Telford MJ. Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Science Advances [Internet]. 2020 Dec [cited 2022 Jan 25]; Available from: https://www.science.org/doi/abs/10.1126/sciadv.abc5162

4. Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, et al. A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals. Current Biology. 2017 Apr 3;27(7):958–67.

5. Jékely G, Budd GE. Animal Phylogeny: Resolving the Slugfest of Ctenophores, Sponges and Acoels? Current Biology. 2021 Feb 22;31(4):R202–4.

6. Whelan NV, Kocot KM, Moroz TP, Mukherjee K, Williams P, Paulay G, et al. Ctenophore relationships and their placement as the sister group to all other animals. Nat Ecol Evol. 2017 Nov;1(11):1737–46.

7. Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, et al. The ctenophore genome and the evolutionary origins of neural systems. Nature. 2014 Jun;510(7503):109–14.

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