Xenacoelomorpha

Xenacoelomorpha
Xenoturbella japonica, a xenacoelomorph member (xenoturbellids)
Proporus sp., another xenacoelomorph member (acoelomorphs)
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Subkingdom:	Eumetazoa
Clade:	ParaHoxozoa
Clade:	Bilateria
Phylum:	Xenacoelomorpha Philippe et al. 2011[1]
Subphyla
Xenoturbellida Acoelomorpha

Xenacoelomorpha^[2] (/ˌzɛnəˌsɛloʊˈmɔːrfə/) is a small phylum of bilaterian invertebrate animals, consisting of two sister groups: xenoturbellids and acoelomorphs. This new phylum was named in February 2011 and suggested based on morphological synapomorphies (physical appearances shared by the animals in the clade),^[3] which was then confirmed by phylogenomic analyses of molecular data (similarities in the DNA of the animals within the clade).^[2][4]

Phylogenetics

Prior to molecular studies, xenacoelomorphs were considered to be flatworms based on their superficial similarities. Like flatworms, they do not have a coelom and are dorsoventrally flattened.^[5] With the advent of phylogenetics, Xenoturbella and Acoelomorpha were found to be sister groups and only distantly related to flatworms.^[4] Initially this phylum was considered to be a member of the deuterostomes,^[2] but because of recent transcriptome analyses, it was concluded that phylum Xenacoelomorpha is the sister group to the Nephrozoa, which includes both the protostomes and the deuterostomes, which makes the phylum the basalmost bilaterian clade.^[6][7] This would mean they are neither deuterostomes nor protostomes.

Bilateria	Xenacoelomorpha Nephrozoa Deuterostomia Ambulacraria Chordata Protostomia Ecdysozoa Spiralia

Their larvae show similarities with cnidarian planula larvae and poriferan parenchyma larvae, but it is not clear if the similarities are ancestral or derived.^[8]

However, some studies point out that their basal placement may be caused by high mutation rates leading to long branch attraction (LBA). These analyses suggest that the xenacoelomorphs are instead the sister group of Ambulacraria forming the clade Xenambulacraria and that despite their simple body plans, they actually derive from a more complex ancestor.^[9][10] Having a larger number of species within this group would allow for better conclusions and analysis to be made within the phylum and in groups closely related to the phylum.

Bilateria	Deuterostomia Xenambulacraria Ambulacraria Xenacoelomorpha Chordata Protostomia Ecdysozoa Spiralia

Internal phylogeny

For multiple decades, the genus Xenoturbella contained only one species, X. bocki. In 2016 however, a team reported the discovery of four new species from the Gulf of California and sequenced each new species' mitogenome and upon analysis found that the two species that lived in shallow water (X. bocki and X. hollandorum) formed a "shallow" clade and that three deep water species formed a "deep" clade.^[11] The following year another team discovered a sixth species, X. japonica, found off the coast of Japan. Their phylogenetic analysis confirmed the first team's hypothesis and placed X. japonica within the shallow clade.^[12]

The other two groups, Nemertodermatida and Acoela, have less clear relationships as species-level phylogenies have not been conducted. Nemertodermatida only has two families and six total genera. Ascopariidae contains two of these genera, while Nemertodermatidae has the other four. A 2016 study analyzed three of the four Nemertodermatid genera and found that Sterreria and Meara are closer to each other than to Nemertoderma, while Nemertinoides was left unplaced.^[6] Acoela phylogeny is even less certain as it is by far the most diverse part of the phylum and is very understudied. A 2011 study attempted to solve this problem and recovered numerous traditional families as polyphyletic. They also recovered a tentative clade of various species from Actinoposthiidae and Isodiametridae which is not shown in the below cladogram.^[13] Several small basal families were not included in their study and their position is still uncertain.

Xenacoelomorpha

Xenoturbella Shallow clade    X. japonica    X. bocki X. hollandorum Deep clade    X. monstrosa    X. churro X. profunda Acoelomorpha Acoela    Actinoposthiidae Antigonariidae Antroposthiidae Diopisthoporidae Nadinidae Paratomellidae Taurididae    Paratomellidae Bursalia Prosopharyngida    Hallangiidae    Hofsteniidae Solenofilomorphidae Crucimusculata    Proporidae    Isodiametridae    Dakuidae Aberrantospermata    Convolutidae Mecynostomidae Nemertodermatida Ascopariidae    Ascoparia Flagellophora Nemertodermatidae    Nemertoderma Nemertinoides    Meara Sterreria

Characteristics

The phylum consists of small, flat and worm-like creatures found in marine and sometimes brackish water environments, on the sediments. There are species that are variously free-living, parasitic, and symbiotic. They can be found at depths of almost 4 km (2.5 mi) and near hydrothermal vents.

The phylum is hermaphroditic (all individuals have both male and female sex organs) and reproduces sexually with direct development, meaning they skip a potentially vulnerable larval stage. Xenoturbella have external fertilization, and Acoelomorpha has internal fertilization.^[14][15][16] All xenacoelomorphs are bilateral, meaning they have a central front-to-back body axis with mirror image right and left sides. They are triploblasts (meaning they have the three germ layers: ectoderm, endoderm, and mesoderm). Their body plan is acoelomate – they lack a coelom – do not have a true body cavity. Also an excretory system is absent, yet all genes related to the excretory system are present except for Osr, which is essential for the development for such a system. In acoelomorphs, which has gone through rapid evolutionary rates and chromosomic rearrangements, about 60% of the genes shared between protostomes and deuterostomes are missing. How many of these genes which are present or absent in Xenoturbella will require a whole genome sequencing.^[17]

While other animals that are diploblastic (only have two germ layers: ectoderm and endoderm) also lack a coelom, those technically do not have an acoelomate body plan because they lack the mesoderm germ layer. In acoels, the mouth opens directly into a large endodermal syncytium, while in nemertodermatids and xenoturbellids there is a sack-like gut lined by unciliated cells.^[18]

A defining feature is a digestive system lacking nerve cells. Because an enteric nervous system, also called the stomatogastric nervous system, is also found in many cnidarians, its absence is most likely a derived trait.^[19]

Their nervous systems are basiepidermal – located right under the epidermis – and they have no brain. The xenoturbellids' nervous system consists of a simple nerve net, with no special concentration of neurons. In acoelomorphs the nervous system is arranged in a series of longitudinal bundles, united in the anterior region by a ring comissure of variable complexity.^[20]

The sensory organs include a statocyst (for balance). Some groups have two unicellular ocelli (simple eyes).^[18][20]

The epidermis of all species within the phylum is ciliated. The cilia are composed of a set of nine pairs of peripheral microtubules and one or two central microtubules (patterns 9+1 and 9+2, respectively). The pairs 4–7 terminate before the tip, creating a structure called a "shelf".^[21]

See also

• List of bilaterial animal orders

References

1. Tyler, S.; Schilling, S.; Hooge, M.; Bush, L.F. (2006–2016). "Xenacoelomorpha". Turbellarian taxonomic database. Version 1.7. Archived from the original on 9 February 2019. Retrieved 3 February 2016.
2. Philippe, H.; Brinkmann, H.; Copley, R. R.; Moroz, L. L.; Nakano, H.; Poustka, A. J.; Wallberg, A.; Peterson, K. J.; Telford, M. J. (10 February 2011). "Acoelomorph flatworms are deuterostomes related to Xenoturbella". Nature. 470 (7333): 255–258. Bibcode:2011Natur.470..255P. doi:10.1038/nature09676. PMC 4025995. PMID 21307940.
3. Lundin, K (1998). "The epidermal ciliary rootlets of Xenoturbella bocki (Xenoturbellida) revisited: new support for a possible kinship with the Acoelomorpha (Platyhelminthes)". Zoologica Scripta. 27 (3): 263–270. doi:10.1111/j.1463-6409.1998.tb00440.x. S2CID 85324766.
4. Hejnol, A.; Obst, M.; Stamatakis, A.; Ott, M.; Rouse, G. W.; Edgecombe, G. D.; et al. (2009). "Assessing the root of bilaterian animals with scalable phylogenomic methods". Proceedings of the Royal Society B: Biological Sciences. 276 (1677): 4261–4270. doi:10.1098/rspb.2009.0896. PMC 2817096. PMID 19759036.
5. What is Xenoturbella? | Zoological Letters - BioMed Central
6. Perseke, M.; Hankeln, T.; Weich, B.; Fritzsch, G.; Stadler, P.F.; Israelsson, O.; Bernhard, D.; Schlegel, M. (August 2007). "The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis" (PDF). Theory Biosci. 126 (1): 35–42. CiteSeerX 10.1.1.177.8060. doi:10.1007/s12064-007-0007-7. PMID 18087755. S2CID 17065867. Archived from the original (PDF) on 24 April 2019. Retrieved 10 December 2013.
7. Cannon, J.T.; Vellutini, B.C.; Smith, J.; Ronquist, F.; Jondelius, U.; Hejnol, A. (4 February 2016). "Xenacoelomorpha is the sister group to Nephrozoa". Nature. 530 (7588): 89–93. Bibcode:2016Natur.530...89C. doi:10.1038/nature16520. PMID 26842059. S2CID 205247296.
8. Nakano, Hiroaki; Lundin, Kennet; Bourlat, Sarah J.; Telford, Maximilian J.; Funch, Peter; Nyengaard, Jens R.; Obst, Matthias; Thorndyke, Michael C. (2013). "Xenoturbella bocki exhibits direct development with similarities to Acoelomorpha". Nature Communications. 4: 1537. Bibcode:2013NatCo...4.1537N. doi:10.1038/ncomms2556. PMC 3586728. PMID 23443565.
9. Philippe, Hervé; et al. (2019). "Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria". Current Biology. 29 (11): 1818–1826.e6. Bibcode:2019CBio...29E1818P. doi:10.1016/j.cub.2019.04.009. hdl:21.11116/0000-0004-DC4B-1. ISSN 0960-9822. PMID 31104936. S2CID 155104811.
10. Kapli, Paschalia; Telford, Maximilian J. (11 December 2020). "Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha". Science Advances. 6 (10): eabc5162. Bibcode:2020SciA....6.5162K. doi:10.1126/sciadv.abc5162. PMC 7732190. PMID 33310849.
11. Rouse, Greg W.; Wilson, Nerida G.; Carvajal, Jose I.; Vrijenhoek, Robert C. (4 February 2016). "New deep-sea species of Xenoturbella and the position of Xenacoelomorpha". Nature. 530 (7588): 94–97. Bibcode:2016Natur.530...94R. doi:10.1038/nature16545. ISSN 0028-0836. PMID 26842060. S2CID 3870574.
12. Nakano, Hiroaki; Miyazawa, Hideyuki; Maeno, Akiteru; Shiroishi, Toshihiko; Kakui, Keiichi; Koyanagi, Ryo; Kanda, Miyuki; Satoh, Noriyuki; Omori, Akihito; Kohtsuka, Hisanori (18 December 2017). "A new species of Xenoturbella from the western Pacific Ocean and the evolution of Xenoturbella". BMC Evolutionary Biology. 17 (1): 245. doi:10.1186/s12862-017-1080-2. ISSN 1471-2148. PMC 5733810. PMID 29249199.
13. Jondelius, Ulf; Wallberg, Andreas; Hooge, Matthew; Raikova, Olga (December 2011). "How the Worm Got its Pharynx: Phylogeny, Classification and Bayesian Assessment of Character Evolution in Acoela". Systematic Biology. 60 (6). doi:10.1093/sysbio/syr073.
14. Pontarotti, Pierre (1 October 2019). Evolution, Origin of Life, Concepts and Methods. Springer Nature. ISBN 978-3-030-30363-1.
15. Nakano, H. (2019). "Development of Xenoturbellida". Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation. Vol. 68. pp. 251–258. doi:10.1007/978-3-030-23459-1_11. ISBN 978-3-030-23458-4. PMID 31598860. S2CID 204033850.
16. Achatz, J. G.; Chiodin, M.; Salvenmoser, W.; Tyler, S.; Martinez, P. (2012). "The Acoela: On their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis)". Organisms, Diversity & Evolution. 13 (2): 267–286. doi:10.1007/s13127-012-0112-4. PMC 3789126. PMID 24098090.
17. Abalde, Samuel; Tellgren-Roth, Christian; Heintz, Julia; Vinnere Pettersson, Olga; Jondelius, Ulf (2023). "The draft genome of the microscopic Nemertoderma westbladi sheds light on the evolution of Acoelomorpha genomes". Frontiers in Genetics. 14: 1244493. doi:10.3389/fgene.2023.1244493. PMC 10565955. PMID 37829276.
18. Achatz, Johannes G.; Chiodin, Marta; Salvenmoser, Willi; Tyler, Seth; Martinez, Pedro (June 2013). "The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis)". Organisms Diversity & Evolution. 13 (2): 267–286. doi:10.1007/s13127-012-0112-4. ISSN 1439-6092. PMC 3789126. PMID 24098090.
19. The digestive system of xenacoelomorphs - CORE
20. Perea-Atienza, E.; Gavilan, B.; Chiodin, M.; Abril, J.F.; Hoff, K.J.; Poustka, A.J.; Martinez, P. (2015). "The nervous system of Xenacoelomorpha: A genomic perspective". Journal of Experimental Biology. 218 (4): 618–628. doi:10.1242/jeb.110379. hdl:2445/192702. ISSN 0022-0949. PMID 25696825.
21. Franzen, Ake; Afzelius, Bjorn A. (January 1987). "The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations". Zoologica Scripta. 16 (1): 9–17. doi:10.1111/j.1463-6409.1987.tb00046.x. ISSN 0300-3256. S2CID 85675105.