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Ecdysozoa

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Ecdysozoa
Temporal range: Cambrian - Recent Possible traces age 556 Ma[1]
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Subkingdom: Eumetazoa
Clade: ParaHoxozoa
Clade: Bilateria
Clade: Nephrozoa
(unranked): Protostomia
Superphylum: Ecdysozoa
Aguinaldo et al., 1997
Phyla

Ecdysozoa (/ˌɛkdɪsoʊˈzoʊə/) is a group of protostome animals,[4] including Arthropoda (insects, chelicerata (including arachnids), crustaceans, and myriapods), Nematoda, and several smaller phyla. The grouping of these animal phyla into a single clade was first proposed by Eernisse et al. (1992) based on a phylogenetic analysis of 141 morphological characters of ultrastructural and embryological phenotypes.[5] This clade, that is, a group consisting of a common ancestor and all its descendants, was formally named by Aguinaldo et al. in 1997, based mainly on phylogenetic trees constructed using 18S ribosomal RNA genes.[6]

A large study in 2008 by Dunn et al. strongly supported the monophyly of Ecdysozoa.[7]

The group Ecdysozoa is supported by many morphological characters, including growth by ecdysis, with moulting of the cuticle – without mitosis in the epidermis – under control of the prohormone ecdysone, and internal fertilization.[8]

The group was initially contested by a significant minority of biologists. Some argued for groupings based on more traditional taxonomic techniques,[9] while others contested the interpretation of the molecular data.[10][11]

Etymology

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The name Ecdysozoa is scientific Greek, derived from ἔκδυσις (ékdusis) "shedding" + ζῷον (zôion) "animal".

Characteristics

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See also: List of bilaterial animal orders

The most notable characteristic shared by ecdysozoans is a three-layered cuticle (four in Tardigrada[12]) composed of organic material, which is periodically molted as the animal grows. This process of molting is called ecdysis, and gives the group its name. The ecdysozoans lack locomotory cilia and produce mostly amoeboid sperm, and their embryos do not undergo spiral cleavage as in most other protostomes. Ancestrally, the group exhibited sclerotized teeth within the foregut, and a ring of spines around the mouth opening, though these features have been secondarily lost in certain groups.[13][14] A respiratory and circulatory system is only present in onychophorans and arthropods (often absent in smaller arthropods like mites); in the rest of the groups, both systems are missing.

Phylogeny

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The Ecdysozoa include the following phyla: Arthropoda, Onychophora, Tardigrada, Kinorhyncha, Priapulida, Loricifera, Nematoda, and Nematomorpha. A few other groups, such as the gastrotrichs, have been considered possible members but lack the main characters of the group, and are now placed elsewhere. The Arthropoda, Onychophora, and Tardigrada have been grouped together as the Panarthropoda because they are distinguished by segmented body plans.[15] Dunn et al. in 2008 suggested that the tardigrada could be grouped along with the nematodes, leaving Onychophora as the sister group to the arthropods.[7] The non-panarthropod members of Ecdysozoa have been grouped as Cycloneuralia but they are more usually considered paraphyletic in representing the primitive condition from which the Panarthropoda evolved.[16]

A modern consensus phylogenetic tree for the protostomes is shown below.[17][18][19][20][21][22] It is indicated when approximately clades radiated into newer clades in millions of years ago (Mya); dashed lines show especially uncertain placements.[23]

The phylogenetic tree is based on Nielsen et al.[24] and Howard et al..[25]

 Bilateria 

Older alternative groupings

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Articulata hypothesis

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The grouping proposed by Aguinaldo et al. is almost universally accepted, replacing an older hypothesis that Panarthropoda should be classified with Annelida in a group called the Articulata, and that Ecdysozoa are polyphyletic. Nielsen has suggested that a possible solution is to regard Ecdysozoa as a sister-group of Annelida,[26] though later considered them unrelated.[27] Inclusion of the roundworms within the Ecdysozoa was initially contested[10][28][29] but since 2003, a broad consensus has formed supporting the Ecdysozoa[30] and in 2011 the Darwin–Wallace Medal was awarded to James Lake for the discovery of the New Animal Phylogeny consisting of the Ecdysozoa, the Lophotrochozoa, and the Deuterostomia.[31]

Coelomata hypothesis

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Before Aguinaldo's Ecdysozoa proposal, one of the prevailing theories for the evolution of the bilateral animals was based on the morphology of their body cavities. There were three types, or grades of organization: the Acoelomata (no coelom), the Pseudocoelomata (partial coelom), and the Eucoelomata (true coelom). Adoutte and coworkers were among the first to strongly support the Ecdysozoa.[32] With the introduction of molecular phylogenetics, the coelomate hypothesis was abandoned, although some molecular, phylogenetic support for the Coelomata continued until as late as 2005.[33]

References

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  1. ^ a b Howard RJ, Giacomelli M, Lozano-Fernandez J, Edgecombe GD, Fleming JF, Kristensen RM, et al. (2022). "The Ediacaran origin of ecdysozoa: Integrating fossil and phylogenomic data". Journal of the Geological Society. 179 (4). Bibcode:2022JGSoc.179..107H. doi:10.1144/jgs2021-107. hdl:2445/186596. S2CID 246494357. Retrieved 2023-07-30.
  2. ^ Liu, Yunhuan; Carlisle, Emily; Zhang, Huaqiao; Yang, Ben; Steiner, Michael; Shao, Tiequan; et al. (17 August 2022). "Saccorhytus is an early ecdysozoan, and not the earliest deuterostome". Nature. 609 (7927): 541–546. Bibcode:2022Natur.609..541L. doi:10.1038/s41586-022-05107-z. hdl:1983/454e7bec-4cd4-4121-933e-abeab69e96c1. ISSN 1476-4687. PMID 35978194. S2CID 251646316.
  3. ^ Howard, Richard J.; Edgecombe, Gregory D.; Shi, Xiaomei; Hou, Xianguang; Ma, Xiaoya (23 November 2020). "Ancestral morphology of Ecdysozoa constrained by an early Cambrian stem group ecdysozoan". BMC Evolutionary Biology. 20 (1): 156. Bibcode:2020BMCEE..20..156H. doi:10.1186/s12862-020-01720-6. ISSN 1471-2148. PMC 7684930. PMID 33228518.
  4. ^ Telford, Maximilian J.; Bourlat, Sarah J.; Economou, Andrew; Papillon, Daniel; Rota-Stabelli, Omar (2008). "The evolution of the Ecdysozoa". Philosophical Transactions of the Royal Society B: Biological Sciences. 363 (1496): 1529–1537. doi:10.1098/rstb.2007.2243. ISSN 0962-8436. PMC 2614232. PMID 18192181.
  5. ^ Eernisse, D.J.; Albert, J.S.; Anderson, F.E. (1992). "Annelida and Arthropoda are not sister taxa: A phylogenetic analysis of spiralian metazoan morphology". Systematic Biology. 41 (3): 305–330. doi:10.1093/sysbio/41.3.305.
  6. ^ Aguinaldo, A.M.A.; Turbeville, J.M.; Linford, L.S.; Rivera, M.C.; Garey, J.R.; Raff, R.A.; Lake, J.A. (29 May 1997). "Evidence for a clade of nematodes, arthropods, and other moulting animals". Nature. 387 (6632): 489–493. Bibcode:1997Natur.387R.489A. doi:10.1038/387489a0. PMID 9168109. S2CID 4334033.
  7. ^ a b Dunn, C.W.; Hejnol, A.; Matus, D.Q.; Pang, K.; Browne, W.E.; Smith, S.A.; et al. (10 April 2008). "Broad phylogenomic sampling improves resolution of the animal tree of life". Nature. 452 (7188): 745–749. Bibcode:2008Natur.452..745D. doi:10.1038/nature06614. PMID 18322464. S2CID 4397099.
  8. ^ Ax, P. (1985). "The position of the Gnathostomulida and Platyhelminthes in the phylogenetic system of the Bilateria". In Conway Morris, S.; George, J.D.; Gibson, R.; Platt, H.M. (eds.). The Origins and Relationships of Lower Invertebrates. Systematics Association Special Volume. Vol. 28. New York, NY: Clarendon / Oxford University Press. pp. 168–180. ISBN 019857181X. OCLC 59186778 – via Internet Archive (archive.org). proceedings of an international symposium held in London, September 1983 ISBN 9780198571810
  9. ^ Nielsen, Claus (1995). Animal Evolution: Interrelationships of the living phyla. Oxford University Press. ISBN 978-0-19-850682-9.
  10. ^ a b Blair, J.E.; Ikeo, Kazuho; Gojobori, Takashi; Hedges, S. Blair (8 April 2002). "The evolutionary position of nematodes". BMC Evolutionary Biology. 2: 7. doi:10.1186/1471-2148-2-7. PMC 102755. PMID 11985779.
  11. ^ Wägele, J.W.; Erikson, T.; Lockhart, P.; Misof, B. (December 1999). "The Ecdysozoa: Artifact or monophylum?". Journal of Zoological Systematics and Evolutionary Research. 37 (4): 211–223. doi:10.1111/j.1439-0469.1999.tb00985.x.
  12. ^ Barnes, Robert D. (1982). Invertebrate Zoology. Philadelphia, PA: Holt-Saunders International. pp. 877–880. ISBN 0-03-056747-5.
  13. ^ Smith, Martin R.; Caron, Jean-Bernard (2 July 2015). "Hallucigenia's head and the pharyngeal armature of early ecdysozoans" (PDF). Nature. 523 (7558): 75–78. Bibcode:2015Natur.523...75S. doi:10.1038/nature14573. PMID 26106857. S2CID 205244325.
  14. ^ Vinther, Jakob; Porras, Luis; Young, Fletcher J.; Budd, Graham E.; Edgecombe, Gregory D. (2016). "The mouth apparatus of the Cambrian gilled lobopodian Pambdelurion whittingtoni". Palaeontology. 59 (6): 841–849. Bibcode:2016Palgy..59..841V. doi:10.1111/pala.12256. hdl:1983/16da11f1-5231-4d6c-9968-69ddc5633a8a.
  15. ^ "Panarthropoda". Paleos (palaeos.com). Invertebrates. Archived from the original on 2007-02-07. Retrieved 17 February 2007.
  16. ^ Webster, Bonnie L.; Copley, Richard R.; Jenner, Ronald A.; Mackenzie-Dodds, Jacqueline A.; Bourlat, Sarah J.; Rota-Stabelli, Omar; et al. (November 2006). "Mitogenomics and phylogenomics reveal priapulid worms as extant models of the ancestral Ecdysozoan". Evolution & Development. 8 (6): 502–510. doi:10.1111/j.1525-142X.2006.00123.x. PMID 17073934. S2CID 22823313.
  17. ^ Edgecombe, Gregory D.; Giribet, Gonzalo; Dunn, Casey W.; Hejnol, Andreas; Kristensen, Reinhardt M.; Neves, Ricardo C.; et al. (June 2011). "Higher-level metazoan relationships: Recent progress and remaining questions". Organisms, Diversity & Evolution. 11 (2): 151–172. doi:10.1007/s13127-011-0044-4. S2CID 32169826.
  18. ^ Fröbius, Andreas C.; Funch, Peter (4 April 2017). "Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans". Nature Communications. 8 (1): 9. Bibcode:2017NatCo...8....9F. doi:10.1038/s41467-017-00020-w. PMC 5431905. PMID 28377584.
  19. ^ Smith, Martin R.; Ortega-Hernández, Javier (2014). "Hallucigenia's onychophoran-like claws and the case for Tactopoda" (PDF). Nature. 514 (7522): 363–366. Bibcode:2014Natur.514..363S. doi:10.1038/nature13576. PMID 25132546. S2CID 205239797.
  20. ^ "Palaeos Metazoa: Ecdysozoa". palaeos.com. Retrieved 2017-09-02.
  21. ^ Yamasaki, Hiroshi; Fujimoto, Shinta; Miyazaki, Katsumi (June 2015). "Phylogenetic position of Loricifera inferred from nearly complete 18S and 28S rRNA gene sequences". Zoological Letters. 1: 18. doi:10.1186/s40851-015-0017-0. PMC 4657359. PMID 26605063.
  22. ^ Nielsen, C. (2002). Animal Evolution: Interrelationships of the Living Phyla (2nd ed.). Oxford University Press. ISBN 0-19-850682-1.
  23. ^ Peterson, Kevin J.; Cotton, James A.; Gehling, James G.; Pisani, Davide (27 April 2008). "The Ediacaran emergence of bilaterians: Congruence between the genetic and the geological fossil records". Philosophical Transactions of the Royal Society of London B: Biological Sciences. 363 (1496): 1435–1443. doi:10.1098/rstb.2007.2233. PMC 2614224. PMID 18192191.
  24. ^ Nielsen, Claus; Brunet, Thibaut; Arendt, Detlev (2018-08-22). "Evolution of the bilaterian mouth and anus". Nature Ecology & Evolution. 2 (9): 1358–1376. Bibcode:2018NatEE...2.1358N. doi:10.1038/s41559-018-0641-0. ISSN 2397-334X. PMID 30135501. S2CID 52067372.
  25. ^ Howard, Richard J.; Giacomelli, Mattia; Lozano-Fernandez, Jesus; Edgecombe, Gregory D.; Fleming, James F.; Kristensen, Reinhardt M.; et al. (10 March 2022). "The Ediacaran origin of Ecdysozoa: Integrating fossil and phylogenomic data". Journal of the Geological Society. 179 (4). Bibcode:2022JGSoc.179..107H. doi:10.1144/jgs2021-107. hdl:2445/186596. ISSN 0016-7649. S2CID 246494357.
  26. ^ Nielsen, C. (September 2003). "Proposing a solution to the Articulata–Ecdysozoa controversy". Zoologica Scripta. 32 (5): 475–482. doi:10.1046/j.1463-6409.2003.00122.x. S2CID 1416582.
  27. ^ Nielsen, Claus (2012). Animal Evolution: Interrelationships of the living phyla (3rd ed.). Oxford University Press. ISBN 978-0-19-960603-0.
  28. ^ Zrzavý, J. (12 January 2002). "Ecdysozoa versus Articulata: Clades, artifacts, prejudices". Journal of Zoological Systematics and Evolutionary Research. 39 (3): 159–163. doi:10.1046/j.1439-0469.2001.00168.x. — in support of clade Ecdysozoa
  29. ^ Wägele, J.W.; Misof, B. (September 2001). "On quality of evidence in phylogeny reconstruction: A reply to Zrzavý's defence of the 'Ecdysozoa' hypothesis". Journal of Zoological Systematics and Evolutionary Research. 39 (3): 165–176. doi:10.1046/j.1439-0469.2001.00177.x.
  30. ^ Telford, Maximilian J.; Littlewood, D. Timothy J. (27 April 2008). "The evolution of the animals: Introduction to a Linnean tercentenary celebration". Philosophical Transactions of the Royal Society B: Biological Sciences. 363 (1496): 1421–1424. doi:10.1098/rstb.2007.2231. PMC 2394567. PMID 18192193.
  31. ^ "The Darwin-Wallace Medal" (Press release). The Linnean Society of London. Retrieved 28 February 2018.
  32. ^ Adoutte, A.; Balavoine, G.; Lartillot, N.; Lespinet, O.; Prud'homme, B.; de Rosa, R. (25 April 2000). "The new animal phylogeny: Reliability and implications". Special feature. Proceedings of the National Academy of Sciences of the USA. 97 (9): 4453–4456. Bibcode:2000PNAS...97.4453A. doi:10.1073/pnas.97.9.4453. PMC 34321. PMID 10781043.
  33. ^ Philip, G.K.; Creevey, C.J.; McInerney, J.O. (9 February 2005). "The Opisthokonta and the Ecdysozoa may not be clades: Stronger support for the grouping of plant and animal than for animal and fungi, and stronger support for the Coelomata than Ecdysozoa". Molecular Biology and Evolution. 22 (5): 1175–1184. doi:10.1093/molbev/msi102. PMID 15703245.
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