By Simran Patel
This is the story of animals who can regenerate body parts1 and house photosynthetic symbionts2. It’s the story of animals you’d mistake for unpaired socks3 living in unexplored places1. If that is not fascinating enough, they could be the closest extant animals to the last bilaterian common ancestor, Ürbilateria. This is the story of Xenacoelomorpha.
Xenacoelomorpha are a phylum of marine hermaphroditic4 bilaterian triploblasts5. They have one opening to the digestive system, i.e. no through gut1. Most have no eyes4, but they do have a nervous system. Xenacoelomorpha evolved rapidly and independently for at least 500 million years6, which you wouldn’t be able to tell from the fact they look like lumps of flesh.
The first phylogenetic analysis placed Xenacoelomorpha at the base of Bilateria in a paraphyletic group, but later this phylum was made a clade4. This clade is made of Xenoturbellida, containing only the genus Xenoturbella, and Acoelomorpha. Xenoturbellida fertilise externally whereas Acoelomorpha fertilise internally; this is reflected in their sperm structures so different it’s hard to believe Xenacoelomorpha is monophyletic7. While Xenoturbellida have a nerve net5, Acoelomorpha have a central nervous system6. Acoelomorpha is further split into Acoela and Nemertodermatida4. Acoela have syncytia with phagocytic vacuoles for a digestive system, while Xenoturbellida and Nemertodermatida have intestines lined with epithelium and basal lamina1. Cryptic species are common though1, such as a population of Paratomella rubra from Spain and England being considered separate species based on mitochondrial gene order8. So, this phylum may remain enigmatic for years to come.
As well as within the phylum, Xenacoelomorpha’s position in animal phylogeny is cryptic. Acoelomorpha was initially classified with flatworms but were deemed too morphologically simple4. Xenoturbella has been placed all over animal phylogeny, from molluscs to hemichordates, based on different evidence. However, one study classifying Xenoturbella with molluscs was contaminated with its bivalve food4, so more evidence is needed to confidently classify this genus. Currently, there are two leading hypotheses for where Xenacoelomorpha stand.
The first hypothesis defines the group Nephrozoa as all bilaterians except Xenacoelomorpha, implying Xenacoelomorpha is the earliest diverging bilaterian clade. Nephrozoa is so called because all bilaterians except Xenacoelomorpha have excretory systems2. This hypothesis is based on the fact that Xenacoelomorpha shares some aspects with non-bilaterians such as having no body cavity, using only cilia for locomotion, and the apparent lack of an excretory system6. On the other hand, Acoelomorpha share a central nervous system and many cell types with bilaterians6.
Bioinformatic evidence for Nephrozoa comes from the sequences of homeobox genes, such as Hox genes, which help determine cell fate9. Brauchle and colleagues found that Xenacoelomorpha have homeobox genes in the same families as bilaterians, some of which are absent from non-bilaterian animals9. However, the acoel Symsagittifera roscoffensis has Hox genes on different chromosomes even though these genes are known for being next to each other in other bilaterians10. Acoel Hox genes aren’t temporally collinear either, meaning they aren’t expressed one after the other like in other bilaterians10. Hence, Xenacoelomorpha has an intermediate homeobox genome to bilaterians and non-bilaterians.
If this hypothesis is true, and Xenacoelomorpha is the sister group to Nephrozoa, features of extant Xenacoelomorpha could be bilaterian ancestral features9. Ürbilateria may have been a small unsegmented acoelomate7, and other bilaterians would have arisen by what many would call an “increase in complexity”. The idea that us humans have evolved from such unappealing worm-like creatures sounds fascinating to many.
However, Xenacoelomorpha being sister to all other bilaterians could be the result of a bioinformatic artifact called Long Branch Attraction11. In models that assume nucleotide substitution rate is equal across sites, taxa with longer branches (more substitutions) on the phylogenetic tree are placed closer together. Because Xenacoelomorpha evolve so quickly8, their phylogenetic branch is very long. This makes tree-making software place the phylum next to the outgroup even if it did not diverge so early11. Another systematic error when constructing phylogenies is compositional bias: a substitution mutation changes the existing amino acid to some amino acids more often than others12. This bias can be reduced by grouping amino acids by R group similarity, recoding protein sequences based on these groups and constructing a phylogeny with these recoded sequences12. Phylogenies made by reducing compositional bias and Long Branch Attraction gave the same conclusion – the Nephrozoa hypothesis is not as likely as previously thought12.
Xenambulacraria is a hypothesis better supported by unbiased phylogenies12 and mitochondrial DNA8. It groups Xenacoelomorpha with echinoderms and hemichordates (together Ambulacraria), implying that Xenacoelomorpha are deuterostomes that lost most of their organs11. Genomic and transcriptomic analysis does reveal Xenacoelomorpha has high rates of gene loss, though the phylogeny the scientists used placed Xenacoelomorpha at the Nephrozoa position13. Another study concluded that Acoelomorpha have lost neuropeptides conserved among animals and GPCRs conserved among bilaterians5, as opposed to other animals gaining and evolving these proteins. Hence, it is plausible that Xenacoelomorpha have lost so many genes that they now look radically different from their starfish sisters. As for morphological evidence supporting this hypothesis, Xenoturbellida sperm has a similar structure to hemichordate sperm but Nemertodermatida sperm structure is more similar to protostomes7. The latter is interesting because a proposed deuterostome sharing something with protostomes could either be the work of convergent evolution or the character state in Ürbilateria7.
Thus, there is evidence for Xenacoelomorpha being sister to either Ambulacraria or all other bilaterians. If the latter is true, they could be key animals in deciphering how bilaterians like us evolved. Xenacoelomorpha is a phylum full of intrigue and controversy, so I’m proud to have told their story.
References:
1. Gavilán B, Sprecher SG, Hartenstein V, et al. The digestive system of xenacoelomorphs. Cell Tissue Res 2019; 377: 369–382.
2. Marlétaz F. Zoology: Worming into the Origin of Bilaterians. Current Biology 2019; 29: R577–R579.
3. Czekanski-Moir JE, Rundell RJ. Endless forms most stupid, icky, and small: The preponderance of noncharismatic invertebrates as integral to a biologically sound view of life. Ecol Evol 2020; 10: 12638–12649.
4. Jondelius U, Raikova OI, Martinez P. Xenacoelomorpha, a Key Group to Understand Bilaterian Evolution: Morphological and Molecular Perspectives. In: Pontarotti P (ed) Evolution, Origin of Life, Concepts and Methods. Cham: Springer International Publishing, pp. 287–315.
5. Thiel D, Franz-Wachtel M, Aguilera F, et al. Xenacoelomorph Neuropeptidomes Reveal a Major Expansion of Neuropeptide Systems during Early Bilaterian Evolution. Molecular Biology and Evolution 2018; 35: 2528–2543.
6. Duruz J, Kaltenrieder C, Ladurner P, et al. Acoel Single-Cell Transcriptomics: Cell Type Analysis of a Deep Branching Bilaterian. Molecular Biology and Evolution 2021; 38: 1888–1904.
7. Buckland-Nicks J, Lundin K, Wallberg A. The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians. Zoomorphology 2019; 138: 13–27.
8. Robertson HE, Lapraz F, Egger B, et al. The mitochondrial genomes of the acoelomorph worms Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae. Sci Rep 2017; 7: 1847.
9. Brauchle M, Bilican A, Eyer C, et al. Xenacoelomorpha Survey Reveals That All 11 Animal Homeobox Gene Classes Were Present in the First Bilaterians. Genome Biology and Evolution 2018; 10: 2205–2217.
10. Gaunt SJ. Hox cluster genes and collinearities throughout the tree of animal life. Int J Dev Biol 2018; 62: 673–683.
11. Kapli P, Telford MJ. Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Science Advances 2020; 6: eabc5162.
12. Philippe H, Poustka AJ, Chiodin M, et al. Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria. Current Biology 2019; 29: 1818-1826.e6.
13. Fernández R, Gabaldón T. Gene gain and loss across the metazoan tree of life. Nat Ecol Evol 2020; 4: 524–533.
Article written in June, 2022
Imperial Bioscience Review 