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Cyclostomi

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"Cyclostomata" redirects here. For the order of bryozoans, see Cyclostomatida.

Cyclostomi
Temporal range: Lochkovian - Recent 419.2–0 Ma
Sea lamprey from Sweden
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Infraphylum: Agnatha
Superclass: Cyclostomi
Duméril, 1806
Classes

Cyclostomi, often referred to as Cyclostomata /sɪkloʊˈstɒmətə/, is a group of vertebrates that comprises the living jawless fishes: the lampreys and hagfishes. Both groups have jawless mouths with horny epidermal structures that function as teeth called ceratodontes, and branchial arches that are internally positioned instead of external as in the related jawed fishes.[1] The name Cyclostomi means "round mouths".[2][3][4] It was named by Joan Crockford-Beattie.[5]

Possible external relationships

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This taxon is often included in the paraphyletic superclass Agnatha, which also includes several groups of extinct armored fishes called ostracoderms. Most fossil agnathans, such as galeaspids, thelodonts, and osteostracans, are more closely related to vertebrates with jaws (called gnathostomes) than to cyclostomes.[6][7]

Biologists historically disagreed on whether cyclostomes are a clade. The "vertebrate hypothesis" held that lampreys are more closely related to gnathostomes than they are to the hagfish. The "cyclostome hypothesis", on the other hand, holds that lampreys and hagfishes are more closely related, making cyclostomi monophyletic.[8][9]

Most studies based on anatomy have supported the vertebrate hypothesis,[10] while most molecular phylogenies have supported the cyclostome hypothesis.[2][8][11][12]

There are exceptions in both cases, however. Similarities in the cartilage and muscles of the tongue apparatus also provide evidence of sister-group relationship between lampreys and hagfishes.[13] And at least one molecular phylogeny has supported the vertebrate hypothesis.[14] The embryonic development of hagfishes was once held to be drastically different from that of lampreys and gnathostomes, but recent evidence suggests that it is more similar than previously thought, which may remove an obstacle to the cyclostome hypothesis.[15]

Several groups of Paleozoic jawless fish have been suggested to be more closely related to cyclostomes than to jawed fish, including conodonts and anaspids. The presence of mineralised elements in these jawless fish, like the oral conodont elements and the armoured body covering of anaspids and scutes on other species like Lasanius suggests that mineralised tissues were present in the last common ancestor of all vertebrates, but were secondarily lost in hagfish and lampreys.[16]

Internal differences and similarities

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Both hagfishes and lampreys have a single gonad, but for different reasons. In hagfishes the left gonad degenerates during their ontogeny and only the right gonad develops, whereas in lampreys the left and right gonads fuse into one. There are no gonoducts present.[17][18]

Hagfishes have direct development, but lamprey go through a larval stage followed by metamorphosis into a juvenile form (or adult form in the non-parasitic species). Lamprey larvae live in freshwater and are called ammocoetes, and are the only vertebrates with an endostyle, an organ used for filter feeding that is otherwise found only in tunicates and lancelets. During metamorphosis the lamprey endostyle develops into the thyroid gland.[19]

The cyclostomi evolved oxygen transport hemoglobins independently from the jawed vertebrates.[20]

Hagfishes and lampreys lack a thymus, spleen, myelin and sympathetic chain ganglia.[21][22][23] Neither species has internal eye muscles and hagfishes also lack external eye muscles.[24] Both groups have only a single olfactory organ with a single nostril. The nasal duct ends blindly in a pouch in lampreys but opens into the pharynx in hagfishes. The branchial basket (reduced in hagfishes) is attached to the cranium.[25]

The common ancestor of both cyclostomes and gnathostomes went through a genome duplication before their split, and while a second genome duplication occurred in the stem-gnathostomes, the stem-cyclostomes experienced an independent genome triplication.[26]

The mouth apparatus in hagfishes and adult lampreys has some similarities, but differ from one another. Lampreys have tooth plates on the top of a tongue-like piston cartilage, and the hagfish have a fixed cartilaginous plate on the floor of its mouth with groves that allows tooth plates to slide backwards and forwards over it like a conveyor belt, and are everted as they move over the edge of the plate. Hagfishes also have a keratinous palatine tooth hanging from the roof of the mouth.[27][28]

Unlike jawed vertebrates, which have three semicircular canals in each inner ear, lampreys have only two and hagfishes just one. The semicircular canal of hagfishes contains both stereocilia and a second class of hair cells, apparently a derived trait, whereas lampreys and other vertebrates have stereocilia only. Because the inner ear of hagfishes has two forms of sensory ampullae, their single semicircular canal is assumed to be a result of two semicircular canals that have merged into just one.

The hagfish blood is isotonic with seawater, while lampreys appears to use the same gill-based mechanisms of osmoregulation as marine teleosts. Yet the same mechanisms are apparent in the mitochondria-rich cells in the gill epithelia of hagfishes, but never develops the ability to regulate the blood's salinity, even if they are capable of regulating the ionic concentration of Ca and Mg ions. It has been suggested that the hagfish ancestors evolved from an anadromous or freshwater species that has since adapted to saltwater over a very long time, resulting in higher electrolyte levels in its blood.[29]

The lamprey intestine has a typhlosole that increases the inner surface like the spiral valve does in some jawed vertebrates. The spiral valve in the latter develops by twisting the whole gut, while the lamprey typhlosole is confined to the mucous membrane of the intestines. The mucous membranes of hagfishes have a primitive typhlosole in the form of permanent zigzag ridges. This trait could be a primitive one, since it is also found in some sea squirts such as Ciona.[30] The intestinal epithelia of lampreys also have ciliated cells, which have not been detected in hagfishes. Because ciliated intestines are also found in Chondrostei, lungfishes and the early stages of some teleosts, it is considered a primitive condition that has been lost in hagfishes.[31]

Phylogeny

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After Miyashita et al. 2019.[32]

References

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  1. ^ The oldest fish in the world lived 500 million years ago | SBS News
  2. ^ a b Kuraku, Shigehiro, S. Blair; Ota, Kinya G. & Kuratani, Shigeru (2009b). "Jawless fishes (Cyclostomata)". In S.B. Hedges & S. Kumar (eds.). Timetree of Life. Oxford University Press. pp. 317–319. ISBN 978-0-19-953503-3.
  3. ^ Haeckel (1895). Systematische Phylogenie der Wirbelthiere (Vertebrata). Entwurf einer systematischen Stammesgeschichte (in German). Vol. 3 (1 ed.). Berlin: Georg Reimer. pp. 142–143.
  4. ^ Duméril, A.M. Constant (1806). Zoologie analytique, ou me´thode naturelle de classification des animaux, Rendue plus facile a l'Aide de Tableaux Synoptiques (in French). Paris: Allais.
  5. ^ Turner, Susan; Beattie, Joan (2008). "Joan Crockford-Beattie D.Sc." (PDF). Annals of Bryozoology 2: Aspects of the History of Research on Bryozoans. 2: viii, 442.
  6. ^ Zhao Wen-Jin; Zhu Min (2007). "Diversification and faunal shift of Siluro-Devonian vertebrates of China". Geological Journal. 42 (3–4): 351–369. Bibcode:2007GeolJ..42..351W. doi:10.1002/gj.1072. S2CID 84943412. Archived from the original on 2013-01-05.
  7. ^ Sansom, Robert S. (2009). "Phylogeny, classification, & character polarity of the Osteostraci (Vertebrata)". Journal of Systematic Palaeontology. 7 (1): 95–115. Bibcode:2009JSPal...7...95S. doi:10.1017/S1477201908002551. S2CID 85924210.
  8. ^ a b Delabre, Christiane; et al. (2002). "Complete Mitochondrial DNA of the Hagfish, Eptatretus burgeri: The Comparative Analysis of Mitochondrial DNA Sequences Strongly Supports the Cyclostome Monophyly". Molecular Phylogenetics and Evolution. 22 (2): 184–192. doi:10.1006/mpev.2001.1045. PMID 11820840.
  9. ^ Stock, David; Whitt GS (7 August 1992). "Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group". Science. 257 (5071): 787–9. Bibcode:1992Sci...257..787S. doi:10.1126/science.1496398. PMID 1496398.
  10. ^ Janvier, Philippe (2003). Early Vertebrates. Oxford University Press. pp. 1–408. ISBN 978-0-19-852646-9.
  11. ^ Kuraku, Shigehiro; Meyer, Axel & Kuratani, Shigeru (2009a). "Timing of Genome Duplications Relative to the Origin of the Vertebrates: Did Cyclostomes Diverge before, or after?". Molecular Biology and Evolution. 26 (1): 47–59. doi:10.1093/molbev/msn222. PMID 18842688.
  12. ^ Heimberg, Alysha M.; Cowper-Sallari, Richard; Sémon, Marie; Donoghue, Philip C. J.; Peterson, Kevin J. (9 November 2010). "microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate". PNAS. 107 (45): 19379–19383. doi:10.1073/pnas.1010350107. PMC 2984222. PMID 20986316.
  13. ^ Yalden, D.M. (1985). "Feeding mechanisms as evidence for cyclostome monophyly". Zoological Journal of the Linnean Society. 84 (3): 291–300. doi:10.1111/j.1096-3642.1985.tb01802.x. Archived from the original on 2013-01-05.
  14. ^ Gürsoy, Halil-Cem; Koper, Dorota; Benecke, Bernd-Joachim (May 2000). "The Vertebrate 7S K RNA Separates Hagfish (Myxine glutinosa) and Lamprey (Lampetra fluviatilis)". Journal of Molecular Evolution. 50 (5): 456–464. Bibcode:2000JMolE..50..456G. doi:10.1007/s002390010048. PMID 10824089. S2CID 9970630.
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  16. ^ Reeves, Jane C.; Wogelius, Roy A.; Keating, Joseph N.; Sansom, Robert S. (March 2023). Cavin, Lionel (ed.). "Lasanius, an exceptionally preserved Silurian jawless fish from Scotland". Palaeontology. 66 (2). Bibcode:2023Palgy..6612643R. doi:10.1111/pala.12643. ISSN 0031-0239.
  17. ^ Webster, Douglas; Webster, Molly (22 October 2013). Comparative Vertebrate Morphology. Academic Press. ISBN 978-1-4832-7259-7.
  18. ^ Khanna, D. R. (2004). Morphogenesis. Discovery Publishing House. ISBN 978-81-7141-771-1.
  19. ^ Torday, John S.; Rehan, Virender K. (21 February 2012). Evolutionary Biology: Cell-Cell Communication, and Complex Disease. John Wiley & Sons. ISBN 978-0-470-64720-2.
  20. ^ "Biologists find that red-blooded vertebrates evolved twice, independently".
  21. ^ Rast, Jonathan P.; Buckley, Katherine M. (2013). "Lamprey immunity is far from primitive". Proceedings of the National Academy of Sciences. 110 (15): 5746–5747. Bibcode:2013PNAS..110.5746R. doi:10.1073/pnas.1303541110. ISSN 0027-8424. PMC 3625256. PMID 23553834.
  22. ^ Gould, Robert M.; Morrison, Hilary; Campbell, Robert; Gilland, Edwin (2004). "Evolution of Myelin Proteins". The Biological Bulletin. 207 (2): 168. doi:10.1086/BBLv207n2p168. PMID 27690608.
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  26. ^ Yu, Daqi; Ren, Yandong; Uesaka, Masahiro; Beavan, Alan J. S.; Muffato, Matthieu; Shen, Jieyu; Li, Yongxin; Sato, Iori; Wan, Wenting; Clark, James W.; Keating, Joseph N.; Carlisle, Emily M.; Dearden, Richard P.; Giles, Sam; Randle, Emma (2024). "Hagfish genome elucidates vertebrate whole-genome duplication events and their evolutionary consequences". Nature Ecology & Evolution. 8 (3): 519–535. Bibcode:2024NatEE...8..519Y. doi:10.1038/s41559-023-02299-z. ISSN 2397-334X. PMC 10927551. PMID 38216617.
  27. ^ Hardisty, M. W. (11 November 2013). Biology of the Cyclostomes. Springer. ISBN 978-1-4899-3408-6.
  28. ^ Hagfish - Cronodon
  29. ^ Foreman, R. E.; Gorbman, A.; Dodd, J. M.; Olsson, R. (9 March 2013). Evolutionary Biology of Primitive Fishes. Springer. ISBN 978-1-4615-9453-6.
  30. ^ "microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate" (PDF). Archived from the original (PDF) on 2016-03-04. Retrieved 2014-04-09.
  31. ^ Fish Physiology: The Multifunctional Gut of Fish. Academic Press. 21 October 2010. ISBN 978-0-08-096136-1.
  32. ^ Miyashita, Tetsuto; Coates, Michael I.; Farrar, Robert; Larson, Peter; Manning, Phillip L.; Wogelius, Roy A.; Edwards, Nicholas P.; Anné, Jennifer; Bergmann, Uwe; Palmer, A. Richard; Currie, Philip J. (2019-02-05). "Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny". Proceedings of the National Academy of Sciences. 116 (6): 2146–2151. Bibcode:2019PNAS..116.2146M. doi:10.1073/pnas.1814794116. ISSN 0027-8424. PMC 6369785. PMID 30670644.
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