Embryonic development in the bonnethead (Sphyrna tiburo), a viviparous hammerhead shark.
craniofacial diversity
evolutionary developmental biology
hammerhead shark
shark embryonic development
staging series
Journal
Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927
Informations de publication
Date de publication:
28 Sep 2023
28 Sep 2023
Historique:
revised:
08
09
2023
received:
10
07
2023
accepted:
09
09
2023
medline:
28
9
2023
pubmed:
28
9
2023
entrez:
28
9
2023
Statut:
aheadofprint
Résumé
The hammerhead sharks (family Sphyrnidae) are an immediately recognizable group of sharks due to their unique head shape. Though there has long been an interest in hammerhead development, there are currently no explicit staging tables published for any members of the group. The bonnethead Sphyrna tiburo is the smallest member of Sphyrnidae and is abundant in estuarine and nearshore waters in the Gulf of Mexico and Western North Atlantic Ocean. Due to their relative abundance, close proximity to shore, and brief gestation period, it has been possible to collect and document multiple embryonic specimens at progressive stages of development. We present the first comprehensive embryonic staging series for the Bonnethead, a viviparous hammerhead shark. Our stage series covers a period of development from stages that match the vertebrate phylotypic period, from Stage 23, through stages of morphological divergence to complete development at birth-Stage 35). Notably, we use a variety of techniques to document crucial stages that lead to their extreme craniofacial diversity, resulting in the formation of one of the most distinctive characters of any shark species, the cephalofoil or hammer-like head. Documenting the development of hard-to-access vertebrates, like this viviparous shark species, offers important information about how new and diverse morphologies arise that otherwise may remain poorly studied. This work will serve as a platform for future comparative developmental research both within sharks and across the phylogeny of vertebrates, underpinning the extreme potential of craniofacial development and morphological diversity in vertebrate animals.
Sections du résumé
BACKGROUND
BACKGROUND
The hammerhead sharks (family Sphyrnidae) are an immediately recognizable group of sharks due to their unique head shape. Though there has long been an interest in hammerhead development, there are currently no explicit staging tables published for any members of the group. The bonnethead Sphyrna tiburo is the smallest member of Sphyrnidae and is abundant in estuarine and nearshore waters in the Gulf of Mexico and Western North Atlantic Ocean. Due to their relative abundance, close proximity to shore, and brief gestation period, it has been possible to collect and document multiple embryonic specimens at progressive stages of development.
RESULTS
RESULTS
We present the first comprehensive embryonic staging series for the Bonnethead, a viviparous hammerhead shark. Our stage series covers a period of development from stages that match the vertebrate phylotypic period, from Stage 23, through stages of morphological divergence to complete development at birth-Stage 35). Notably, we use a variety of techniques to document crucial stages that lead to their extreme craniofacial diversity, resulting in the formation of one of the most distinctive characters of any shark species, the cephalofoil or hammer-like head.
CONCLUSION
CONCLUSIONS
Documenting the development of hard-to-access vertebrates, like this viviparous shark species, offers important information about how new and diverse morphologies arise that otherwise may remain poorly studied. This work will serve as a platform for future comparative developmental research both within sharks and across the phylogeny of vertebrates, underpinning the extreme potential of craniofacial development and morphological diversity in vertebrate animals.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 The Authors. Developmental Dynamics published by Wiley Periodicals LLC on behalf of American Association for Anatomy.
Références
Gilbert CR. A revision of the hammerhead sharks (family Sphyrnidae). Proc US Natl Mus. 1967;119(3539):1-88. doi:10.5479/si.00963801.119-3539.1
Compagno LJV. Sharks of the Order Carcharhiniformes. Princeton University Press; 1988.
Mara KR, Motta PJ, Martin AP, Hueter RE. Constructional morphology within the head of hammerhead sharks (sphyrnidae): cranial morphology in hammerhead sharks. J Morph. 2015;276(5):526-539. doi:10.1002/jmor.20362
Naylor GJP. The phylogenetic relationships among requiem and hammerhead sharks: inferring phylogeny when thousands of Most parsimonious trees result. Cladistics. 1992;8(4):295-318. doi:10.1111/j.1096-0031.1992.tb00073.x
Lim DD, Motta P, Mara K, Martin AP. Phylogeny of hammerhead sharks (family Sphyrnidae) inferred from mitochondrial and nuclear genes. Mol Phylogenet Evol. 2010;55(2):572-579. doi:10.1016/j.ympev.2010.01.037
Kajiura SM, Holland KN. Electroreception in juvenile scalloped hammerhead and sandbar sharks. J Exp Biol. 2002;205(23):3609-3621. doi:10.1242/jeb.205.23.3609
Gaylord MK, Blades EL, Parsons GR. A hydrodynamics assessment of the hammerhead shark cephalofoil. Sci Rep. 2020;10(1):14495. doi:10.1038/s41598-020-71472-2
Kajiura SM, Forni JB, Summers AP. Olfactory morphology of carcharhinid and sphyrnid sharks: does the cephalofoil confer a sensory advantage? J Morphol. 2005;264(3):253-263. doi:10.1002/jmor.10208
Rygg AD, Cox JPL, Abel R, Webb AG, Smith NB, Craven BA. A computational study of the hydrodynamics in the nasal region of a hammerhead shark (Sphyrna tudes): implications for olfaction. PLoS One. 2013;8(3):e59783. doi:10.1371/journal.pone.0059783
McComb DM, Tricas TC, Kajiura SM. Enhanced visual fields in hammerhead sharks. J Exp Biol. 2009;212(24):4010-4018. doi:10.1242/jeb.032615
Setna S, Sarangdhar P. Studies on the development of some Bombay elasmobranchs. Rec Ind Mus. 1949;47(12):203-216.
Appukuttan KK. Studies on the developmental stages of hammerhead shark Sphyrna (eusphyrna) blochii from the Gulf of Mannar. Indian J Fish. 1978;25:41-52.
De Beer GR. The development of the skull of Scyllium (Scyliorhinus) canicula L. J Cell Sci. 1931;2(296):591-646.
El-Toubi MR. The development of the chondrocranium of the spiny dogfish, Acanthias vulgaris (Squalus acanthias). Part I. Neurocranium, mandibular and hyoid arches. J Morphol. 1949;84(2):227-279. doi:10.1002/jmor.1050840204
Ballard WW, Mellinger J, Lechenault H. A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish(Chondrichthyes: Scyliorhinidae). J Exp Zool. 1993;267(3):318-336. doi:10.1002/jez.1402670309
Grunow B, Reismann T, Moritz T. Pre-hatching ontogenetic changes of morphological characters of small-spotted catshark (Scyliorhinus canicula). Fishes. 2022;7(3):100. doi:10.3390/fishes7030100
Maxwell EE, Fröbisch NB, Heppleston AC. Variability and conservation in late chondrichthyan development: ontogeny of the winter skate (Leucoraja ocellata). Anat Rec. 2008;291(9):1079-1087. doi:10.1002/ar.20719
Gillis JA, Bennett S, Criswell KE, et al. Big insight from the little skate: Leucoraja erinacea as a developmental model system. Curr Top Dev Biol. 2022;147:595-630. doi:10.1016/bs.ctdb.2021.12.016
Castro JI, Wourms JP. Reproduction, placentation, and embryonic development of the Atlantic sharpnose shark, Rhizoprionodon terraenovae. J Morphol. 1993;218(3):257-280. doi:10.1002/jmor.1052180304
Onimaru K, Motone F, Kiyatake I, Nishida K, Kuraku S. A staging table for the embryonic development of the brownbanded bamboo shark (Chiloscyllium punctatum): bamboo shark development. Dev Dyn. 2018;247(5):712-723. doi:10.1002/dvdy.24623
Lopez-Romero FA, Klimpfinger C, Tanaka S, Kriwet J. Growth trajectories of prenatal embryos of the deep-sea shark Chlamydoselachus anguineus (Chondrichthyes). J Fish Biol. 2020;97(1):212-224. doi:10.1111/jfb.14352
Coolen M, Menuet A, Chassoux D, et al. The Dogfish Scyliorhinus canicula: a reference in jawed vertebrates. Cold Spring Harb Protoc. 2008;2008(12):pdb-emo111. doi:10.1101/pdb.emo111
Godard BG, Mazan S. Early patterning in a chondrichthyan model, the small spotted dogfish: towards the gnathostome ancestral state. J Anat. 2013;222(1):56-66. doi:10.1111/j.1469-7580.2012.01552.x
López-Romero FA, Berio F, Abed-Navandi D, Kriwet J. Early shape divergence of developmental trajectories in the jaw of galeomorph sharks. Front Zool. 2022;19(1):7. doi:10.1186/s12983-022-00452-1
Richardson MK. Heterochrony and the phylotypic period. Dev Biol. 1995;172(2):412-421. doi:10.1006/dbio.1995.8041
Buddle AL, Van Dyke JU, Thompson MB, Simpfendorfer CA, Whittington CM. Evolution of placentotrophy: using viviparous sharks as a model to understand vertebrate placental evolution. Mar Freshw Res. 2019;70(7):908. doi:10.1071/MF18076
Pollom R, Carlson J, Charvet P, et al. Sphyrna tiburo. The IUCN Red List of Threatened Species 2021: e.T39387A205765567. Published online July 2, 2019 2023. doi:10.2305/IUCN.UK.2021-3.RLTS.T39387A205765567.en
Manire CA, Rasmussen LEL, Hess DL, Hueter RE. Serum steroid hormones and the reproductive cycle of the female Bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol. 1995;97(3):366-376. doi:10.1006/gcen.1995.1036
Lombardi-Carlson LA, Cortés E, Parsons GR, Manire CA. Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo, (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico. Mar Freshw Res. 2003;54(7):875. doi:10.1071/MF03023
Gonzalez De Acevedo M, Frazier BS, Belcher C, Gelsleichter J. Reproductive cycle and fecundity of the bonnethead Sphyrna tiburo L. from the Northwest Atlantic Ocean. J Fish Biol. 2020;97(6):1733-1747. doi:10.1111/jfb.14537
Leuckart FS. Untersuchungen Über Die Äusseren Kiemen Der Embryonen von Rochen Und Hayen: Ein Beitrag Zur Entwicklungsgeschichte Der Der Abtheilung Der Knorpelfische Angehörenden Plagiostomen. LF Rieger; 1836.
Schlernitzauer DA, Gilbert PW. Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo. J Morphol. 1966;120(3):219-231. doi:10.1002/jmor.1051200302
Didier DA, LeClair EE, Vanbuskirk DR. Embryonic staging and external features of development of the Chimaeroid fish, Callorhinchus milii (Holocephali, Callorhinchidae). J Morphol. 1998;236(1):25-47.
Grover CA. Juvenile denticles of the swell shark Cephaloscyllium ventriosum: function in hatching. Can J Zool. 1974;52(3):359-363. doi:10.1139/z74-043
Johanson Z, Smith MM, Joss JMP. Early scale development in Heterodontus (Heterodontiformes; Chondrichthyes): a novel chondrichthyan scale pattern. Acta Zool. 2007;88(3):249-256. doi:10.1111/j.1463-6395.2007.00276.x
Cooper RL, Thiery AP, Fletcher AG, Delbarre DJ, Rasch LJ, Fraser GJ. An ancient Turing-like patterning mechanism regulates skin denticle development in sharks. Sci Adv. 2018;4(11). doi:10.1126/sciadv.aau5484
Cooper RL, Nicklin EF, Rasch LJ, Fraser GJ. Teeth outside the mouth: The evolution and development of shark denticles. Evol Dev. 2023;25(1):54-72. doi:10.1111/ede.12427
Wheeler CR, Rummer JL, Bailey B, Lockwood J, Vance S, Mandelman JW. Future thermal regimes for epaulette sharks (Hemiscyllium ocellatum): growth and metabolic performance cease to be optimal. Sci Rep. 2021;11(1):454. doi:10.1038/s41598-020-79953-0
Parsons GR. Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo. Environ Biol Fishes. 1993;38:25-35.
Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development. 1994;1994(Supplement):135-142. doi:10.1242/dev.1994.Supplement.135
Irie N, Kuratani S. The developmental hourglass model: a predictor of the basic body plan? Development. 2014;141(24):4649-4655. doi:10.1242/dev.107318
Gabner S, Böck P, Fink D, Glösmann M, Handschuh S. The visible skeleton 2.0: phenotyping of cartilage and bone in fixed vertebrate embryos and foetuses based on X-ray microCT. Development. 2020;147(11):dev187633. doi:10.1242/dev.187633
Dingerkus G, Uhler LD. Enzyme clearing of Alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol. 1977;52(4):229-232. doi:10.3109/10520297709116780