The remarkable dynamics in the establishment, rearrangement, and loss of dentition during the ontogeny of the sterlet sturgeon
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
Wellcome Trust - United Kingdom
PubMed
34846759
DOI
10.1002/dvdy.444
Knihovny.cz E-zdroje
- Klíčová slova
- Acipenser, non-teleost fishes, odontogenesis, teeth patterning, tooth development,
- MeSH
- biologická evoluce MeSH
- dentice * MeSH
- obratlovci MeSH
- odontogeneze MeSH
- ryby MeSH
- zuby * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: Sturgeons belong to an early-branching lineage often used as a proxy of ancestor-like traits of ray-finned fishes. However, many features of this lineage, such as the transitory presence and the eventual loss of dentition, exemplify specializations that, in fact, provide important information on lineage-specific evolutionary dynamics. RESULTS: Here, we introduce a detailed overview of the dentition during the development of the sterlet sturgeon. The dentition is composed of tooth fields at oral, palatal, and anterior pharyngeal regions. Oral fields are single-rowed, non-renewed and are shed early. Palatal and pharyngeal fields are multi-rowed and renewed from the adjacent superficial epithelium without the presence of the successional dental lamina. The early loss of oral fields and subsequent establishment of palatal and pharyngeal fields leads to a translocation of the functional dentition from the front to the rear of the oropharyngeal cavity until the eventual loss of all teeth. CONCLUSIONS: Our survey shows the sterlet dentition as a dynamic organ system displaying differential composition at different time points in the lifetime of this fish. These dynamics represent a conspicuous feature of sturgeons, unparalleled among extant vertebrates, and appropriate to scrutinize developmental and evolutionary underpinnings of vertebrate odontogenesis.
Department of Evolutionary Biology University of Vienna Vienna Austria
Department of Zoology Faculty of Science Charles University Prague Czech Republic
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Fraser GJ, Hulsey CD, Bloomquist RF, Uyesugi K, Manley NR, Streelman JT. An ancient gene network is co-opted for teeth on old and new jaws. PLoS Biol. 2009;7(2):e31. doi:10.1371/journal.pbio.1000031
Rücklin M, Donoghue PCJ, Johanson Z, Trinajstic K, Marone F, Stampanoni M. Development of teeth and jaws in the earliest jawed vertebrates. Nature. 2012;491:748-751. doi:10.1038/nature11555
Qu Q, Haitina T, Zhu M, Ahlberg P. New genomic and fossil data illuminate the origin of enamel. Nature. 2015;526:108-111. doi:10.1038/nature15259
Chen D, Blom H, Sanchez S, Tafforeau P, Ahlberg P. The stem osteichthyan Andreolepis and the origin of tooth replacement. Nature. 2016;539:237-241. doi:10.1038/nature19812
Vaškaninová V, Chen D, Tafforeau P, et al. Marginal dentition and multiple dermal jawbones as the ancestral condition of jawed vertebrates. Science. 2020;369(6500):211-216. doi:10.1126/science.aaz9431
Van der Heyden C, Huysseune A. Dynamics of tooth formation and replacement in the zebrafish (Danio rerio) (Teleostei, Cyprinidae). Dev Dyn. 2000;219(4):486-496. doi:10.1002/1097-0177(2000)9999:9999<::AID-DVDY1069>3.0.CO;2-Z
Debiais-Thibaud M, Borday-Birraux V, Germon I, et al. Development of oral and pharyngeal teeth in the medaka (Oryzias latipes): comparison of morphology and expression of eve1 gene. J Exp Zool B Mol Dev Evol. 2007;308(6):693-708. doi:10.1002/jez.b.21183
Atukorala ADS, Franz-Odendaal TA. Spatial and temporal events in tooth development of Astyanax mexicanus. Mech Dev. 2014;134:42-54. doi:10.1016/j.mod.2014.09.002
Ellis NA, Donde NN, Miller CT. Early development and replacement of the stickleback dentition. J Morphol. 2016;277(8):1072-1083. doi:10.1002/jmor.20557
Vandenplas S, De Clercq A, Huysseune A. Tooth replacement without a dental lamina: the search for epithelial stem cells in Polypterus senegalus. J Exp Zool B Mol Dev Evol. 2014;322(5):281-293. doi:10.1002/jez.b.22577
Vandenplas S, Willems M, Witten PE, Hansen T, Fjelldal PG, Huysseune A. Epithelial label-retaining cells are absent during tooth cycling in Salmo salar and Polypterus senegalus. PLoS One. 2016;11(4):e0152870. doi:10.1371/journal.pone.0152870
Smith MM, Johanson Z, Butts T, et al. Making teeth to order: conserved genes reveal an ancient molecular pattern in paddlefish (Actinopterygii). Proc R Soc B. 1805;2015(282):20142700. doi:10.1098/rspb.2014.2700
Clemen G, Bartsch P, Wacker K. Dentition and dentigerous bones in juveniles and adults of Polypterus senegalus (Cladistia, actinopterygii). Ann Anat. 1998;180(3):211-221. doi:10.1016/S0940-9602(98)80076-9
Wacker K, Bartsch P, Clemen G. The development of the tooth pattern and dentigerous bones in Polypterus senegalus (Cladistia, Actinopterygii). Ann Anat. 2001;183(1):37-52. doi:10.1016/S0940-9602(01)80011-X
Jarvik E. On the visceral skeleton in Eusthenopteron, with a discussion of the parasphenoid and palatoquadrate in fishes. Kungl Svenska Vetenskakad Handl. 1954;5:1-104.
Nelson GJ. Gill arches and the phylogeny of fishes: with notes on the classification of vertebrates. Bull Am Mus Nat Hist. 1969;141:479-552.
Smith MM, Coates MI. Evolutionary origins of the vertebrate dentition: phylogenetic patterns and developmental evolution. Eur J Oral Sci. 1998;106 (Suppl 1):482-500. doi:10.1111/j.1600-0722.1998.tb02212.x
Donoghue PCJ. Evolution of development of the vertebrate dermal and oral skeletons: unraveling concepts, regulatory theories, and homologies. Paleobiology. 2002;28:474-507. doi:10.1666/0094-8373(2002)028<0474:EODOTV>2.0.CO;2
Warth P, Hilton EJ, Naumann B, Olsson L, Konstantinidis P. Development of the skull and pectoral girdle in Siberian sturgeon, Acipenser baerii, and Russian sturgeon, Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae). J Morphol. 2017;278(3):418-442. doi:10.1002/jmor.20653
Jollie M. Development of head and pectoral girdle skeleton and scales in Acipenser. Copeia. 1980;1980(2):226-249. doi:10.2307/1444000
Bemis WE, Findeis EK, Grande L. An overview of Acipenseriformes. Envir Biol Fishes. 1997;48(1):25-71. doi:10.1023/A:1007370213924
Hilton E, Grande L, Bemis W. Skeletal anatomy of the shortnose sturgeon, Acipenser brevirostrum Lesueur, 1818, and the systematics of sturgeons (Acipenseriformes, Acipenseridae). Fieldiana Life Earth Sci. 2011;3:1-168. doi:10.3158/2158-5520-3.1.1
Grande L, Bemis WE. Osteology and phylogenetic relationships of fossil and recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes. J Vert Paleo. 1991;11(Supp 1):1-121. doi:10.1080/02724634.1991.10011424
Imms AD. Notes on the gill-rakers of the spoonbill sturgeon, Polyodon spathula. Proc Zool Soc London. 1904;74:22-35.
Carroll AM, Wainwright PC. Functional morphology of prey capture in the sturgeon, Scaphirhynchus albus. J Morphol. 2003;256(3):270-284. doi:10.1002/jmor.10095
Miller M. The ecology and functional morphology of feeding of North American sturgeon and paddlefish. Fish Fish Ser. 2004;27:87-102. doi:10.1007/1-4020-2833-4_5
Warth P, Hilton EJ, Naumann B, Olsson L, Konstantinidis P. Development of the muscles associated with the mandibular and hyoid arches in the Siberian sturgeon, Acipenser baerii (Acipenseriformes: Acipenseridae). J Morphol. 2018;279(2):163-175. doi:10.1002/jmor.20761
Keränen SV, Kettunen P, Aberg T, Thesleff I, Jernvall J. Gene expression patterns associated with suppression of odontogenesis in mouse and vole diastema regions. Dev Genes Evol. 1999;209(8):495-506. doi:10.1007/s004270050282
Fraser GJ, Graham A, Smith MM. Conserved deployment of genes during odontogenesis across osteichthyans. Proc R Soc B. 2004;271(1555):2311-2317. doi:10.1098/rspb.2004.2878
Fraser GJ, Bloomquist RF, Streelman JT. A periodic pattern generator for dental diversity. BMC Biol. 2008;6(1):32. doi:10.1186/1741-7007-6-32
Stock DW, Jackman WR, Trapani J. Developmental genetic mechanisms of evolutionary tooth loss in cypriniform fishes. Development. 2006;133(16):3127-3137. doi:10.1242/dev.02459
Debiais-Thibaud M, Chiori R, Enault S, et al. Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system. BMC Evol Biol. 2015;15:292. doi:10.1186/s12862-015-0557-0
Rasch LJ, Martin KJ, Cooper RL, Metscher BD, Underwood CJ, Fraser GJ. An ancient dental gene set governs development and continuous regeneration of teeth in sharks. Dev Biol. 2016;415(2):347-370. doi:10.1016/j.ydbio.2016.01.038
Soukup V, Tazaki A, Yamazaki Y, et al. Oral and palatal dentition of axolotl arises from a common tooth-competent zone along the ecto-endodermal boundary. Front Cell Dev Biol. 2021;8:1655. doi:10.3389/fcell.2020.622308
Witten PE, Villwock W. Growth requires bone resorption at particular skeletal elements in a teleost fish with acellular bone (Oreochromis niloticus, Teleostei: Cichlidae). J Appl Ichthyol. 1997;13(4):149-158. doi:10.1111/j.1439-0426.1997.tb00115.x
Findeis EK. Osteology and phylogenetic interrelationships of sturgeons (Acipenseridae). Env Biol Fishes. 1997;48(1):73-126. doi:10.1023/A:1007372832213
Fieszl J, Bogacka-Kapusta E, Kapusta A, Szymańska U, Martyniak A. Feeding ecology of sterlet Acipenser ruthenus L. in the Hungarian section of the Danube River. Arch Pol Fish. 2011;19(3):105-111. doi:10.2478/v10086-011-0012-9
Muir WD GT Jr, Parsley MJ, Hinton SA. Diet of first-feeding larval and young-of-the-year white sturgeon in the lower Columbia River. Northwest Sci. 2000;74:25-33.
China V, Holzman R. Hydrodynamic starvation in first-feeding larval fishes. Proc Nat Acad Sci of USA. 2014;111:8083-8088. doi:10.1073/pnas.1323205111
Dial TR, Lauder GV. Longer development provides first-feeding fish time to escape hydrodynamic constraints. J Morphol. 2020;281(8):956-969. doi:10.1002/jmor.21224
Boglione C, Bronzi P, Cataldi E, Serra S, Gagliardi F, Cataudella S. Aspects of early development in the Adriatic sturgeon Acipenser naccarii. J Appl Ichthyol. 1999;15:207-213. doi:10.1111/j.1439-0426.1999.tb00236.x
Piotrowska I, Szczepkowska B, Kozłowski M, Wunderlich K, Szczepkowski M. Results of the larviculture of Atlantic sturgeon (Acipenser oxyrinchus) fed different types of diets. Arch Pol Fish. 2013;21(1):53-61. doi:10.2478/aopf-2013-0006
Underwood CJ, Johanson Z, Welten M, et al. Development and evolution of dentition pattern and tooth order in the skates and rays (Batoidea; Chondrichthyes). PLoS One. 2015;10(4):e0122553. doi:10.1371/journal.pone.0122553
Underwood C, Johanson Z, Smith MM. Cutting blade dentitions in squaliform sharks form by modification of inherited alternate tooth ordering patterns. Roy Soc Open Sci. 2016;3(11):160385. doi:10.1098/rsos.160385
Fraser G, Standing A, Underwood C, Thiery A. The dental lamina: an essential structure for perpetual tooth regeneration in sharks. Integr Comp Biol. 2020;60(3):644-655. doi:10.1093/icb/icaa102
Martin K, Rasch L, Cooper R, Metscher B, Johanson Z, Fraser G. Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles. Proc Natl Acad Sci U S A. 2016;113:201612354. doi:10.1073/pnas.1612354113
Rasch LJ, Cooper RL, Underwood C, Dillard WA, Thiery AP, Fraser GJ. Development and regeneration of the crushing dentition in skates (Rajidae). Dev Biol. 2020;466(1):59-72. doi:10.1016/j.ydbio.2020.07.014
Fraser GJ, Cerny R, Soukup V, Bronner-Fraser M, Streelman JT. The odontode explosion: the origin of tooth-like structures in vertebrates. Bioessays. 2010;32(9):808-817. doi:10.1002/bies.200900151
Reif WE. Evolution of dermal skeleton and dentition in vertebrates. In: Hecht MK, Wallace B, Prance GT, eds. Evolutionary Biology. Vol 15. Boston, MA: Springer; 1982:287-368. doi:10.1007/978-1-4615-6968-8_7
Smith MM, Fraser GJ, Mitsiadis TA. Dental lamina as source of odontogenic stem cells: evolutionary origins and developmental control of tooth generation in gnathostomes. J Exp Zool B Mol Dev Evol. 2009;312B(4):260-280. doi:10.1002/jez.b.21272
Whitlock JA, Richman JM. Biology of tooth replacement in amniotes. Int J Oral Sci. 2013;5(2):66-70. doi:10.1038/ijos.2013.36
Berkovitz BKB. Chronology of tooth development in the rainbow trout (Salmo gairdneri). J Exp Zool. 1977;200(1):65-69. doi:10.1002/jez.1402000109
Huysseune A, Witten PE. An evolutionary view on tooth development and replacement in wild Atlantic salmon (Salmo salar L.). Evol Dev. 2008;10(1):6-14. doi:10.1111/j.1525-142X.2007.00209.x
Square TA, Sundaram S, Mackey EJ, Miller CT. Distinct tooth regeneration systems deploy a conserved battery of genes. EvoDevo. 2021;12(1):4. doi:10.1186/s13227-021-00172-3
Minarik M, Stundl J, Fabian P, et al. Pre-oral gut contributes to facial structures in non-teleost fishes. Nature. 2017;547:209-212. doi:10.1038/nature23008
Rizzato PP, Pospisilova A, Hilton EJ, Bockmann FA. Ontogeny and homology of cranial bones associated with lateral-line canals of the Senegal bichir, Polypterus senegalus (Actinopterygii: Cladistii: Polypteriformes), with a discussion on the formation of lateral-line canal bones in fishes. J Anat. 2020;237(3):439-467. doi:10.1111/joa.13202
Connolly MH, Yelick P. High-throughput methods for visualizing the teleost skeleton: capturing autofluorescence of alizarin red. J Appl Ichthyol. 2010;26(2):274-277. doi:10.1111/J.1439-0426.2010.01419.X