Eugnathostomata, Chondrichthyes, and "spiny sharks"
All contemporary analyses agree that the living gnathostomes:
- Chondrichthyes: the cartilaginous fish
- Osteichthyes: the bony fish
From the SUNY Orange
- The myomeres of lampreys (right) and hagfish are continuous from top to bottom. Those of living gnathostomes are divided into dorsal and ventral blocks by a horizontal septum of connective tissue. (See transverse cross-section). Trinajstic et al., 2007 describing fossils with exceptional soft tissue preservation show that arthrodires and ptychtodontids, like lampreys, lacked the horizontal septum.
Alternative palatoquadrate articulations with neurocranium
(Few have all of these.) - Palatoquadrate articulates with neurocranium dorsally. (In placoderm-grade gnathostomes it was attached to the medial surface of the dermal bones of the skull roof.)
- Primary jaw adductor muscle mass is lateral to the mandibular arch. (Among placoderm-grade gnathostomes, the palatoquadrate is attached to the dermal skull roof, and the jaw muscles pass medially to it.)
Lower dentition of Heterodontus - Teeth: Odontodes of the oral cavity anchored either in soft tissue around palatoquadrate and Meckel's cartilage, or in dermal bone at margin of mouth. We have seen their putative precursors in Thelodonti and placoderm-grade gnathostomes. In Eugnathostomata we finally see oral odontodes that all researchers are comfortable in regarding as homologous. Their features:
- Subject to regular replacement, causing them either to be shed or to accumulate in whorls.
- Bearing outer layer of enamel (interlocking apatite crystals without organic matrix). Note, tooth formation requires inductive interaction of mesodermal odontoblasts to produce dentin and pulp cavity and ectodermal ameloblasts to produce enamel.
Dorsal view of Placoderm (left) and eugnathostome (right) braincases after Schultze, 1993. - Loss of anterior neurocranial fissure (between ethmoid region and remainder of neurocranium)
Lateral view of Placoderm (above) and eugnathostome (below) braincases after Schultze, 1993. - Incomplete fusion of the occipital arch and otic region results in a lateral otic fissure through which cranial nerve X passes. (Equals metotic fissure of some authors.)
Ventral view of Placoderm (left) and eugnathostome (right) braincases after Schultze, 1993. - Elongation of the sphenoid region with respect to the otico-occipital region. In placoderms, the otico-occipital region can take up up to 3/4 the length of the neurocranium. In Eugnathostomes, this is reduced.
Mimipiscis neurocranium - Ventral cranial fissure in floor of braincase between otic (parachordal) and sphenoid (trabecular) regions. (Note: This feature is usually associated with Osteichthyes, but has recently been observed in the stem chondrichthyan Pucapampella (Maisey and Anderson, 2001).)
- Amphistylic suspension of palatoquadrate: Palatoquadrate articulates with neurocranium both directly and via hyomandibula.
Eugnathostome diversity:
Osteichthyes: Wedgetail triggerfish Rhinecanthus rectangulus (right); Chondrichthyes: Blue-spotted lagoon ray Taeniura lymna (left)
Two major living groups:
- Chondrichthyes (Silurian - Quaternary) - Living cartilaginous fish and their fossil relatives
- Osteichthyes (Silurian - Quaternary) - living bony fish and their fossil relatives
Chondrichthyes
Triakis semifasciata (Neoselachii) from Environmental Aquatic Service International
Hydrolagus colliei (Chimaeriformes) from Takako Uno
Living chondrichthyan diversity include:
- Chimaeriformes: (Carboniferous - Quaternary) Chimaeras and fossil relatives
- Neoselachii: (Triassic - Quaternary) Shark-like chondrichthyans.
Dorsal view of Xenacanthus sp. braincase
after Schultze, 1993.
- Prismatic perichondral calcification of the cartilage: It is often said that chondrichthyans lack internal bone. While true, it is not quite diagnostic. Unlike bone, prismatic calcification takes the form of chains of tiny apatite crystals covering the surface of cartilage, linked together by collagen. Note: Chondrichthyans do not lack other hard tissues. Various groups make teeth, fin spines, and dermal armor out of dentine and enamel. Finally, bone is present as a component of scales.
- Precerebral fontanelle: A trough-like dorsal opening in the ethmoid region medial to the nasal capsules (right).
- Lateral otic process of the otic region (right).
- Eugnathostome ventral cranial fissure and lateral otic fissure are secondarily closed.
- Teeth develop as whorls anchored directly in palatoquadrate or Meckel's cartilage with new teeth being added medially, migrating to a functional position, then being shed laterally. (Dearden and Giles, 2021)
- Claspers on pelvic fins as intromittant organs.
Chondrichthyan diversity
Stem chondrichthyans: The earliest unambiguous chondrichthyan remains are from the Early Silurian, but consist of isolated scales. (Possible chondrichthyan scales extend into the Late Ordovician.) We pick up relatively complete fossil chondrichthyans during the Devonian, however their first great radiation occurred during the Early Carboniferous. Alas, there is much disagreement about the phylogeny of basal chondrichthyans. Our review is based on Coates et al., 2017. The cladogram at right provides a consensus of recent hypotheses. Euchondrichthyes (Pradel et al., 2011) is the last common ancestor of living chondrichthyans and all of its descendants. We consider the living groups first, then try to make sense of the stem taxa.
Elasmobranchii:
(Devonian - Quaternary) Chondrichthyans closer to living sharks than to living chimaeras. The cladogram (right) presents a general consensus of elasmobranch phylogeny.Synapomorphies:
- Vertebral column in which arcualia form distinct neural arches that are inserted into the notochord.
- Hypobranchial elements of branchial arches point posteriorly. (Contrast with osteichthyan pattern.)
- Cladodont teeth ancestrally - One tall central cusp is flanked by smaller cusplets.
- Pectoral fin skeleton formed around:
- three basals (cartilage)
- numerous radials (cartilage)
- ceratotrichia (keratin)
Elasmobranch diversity:
Xenacanthida: (Carboniferous (or Devonian?) - Triassic)Predators with elongate bodies. During the Carboniferous and Permian, they were among the top marine predators. After the end Permian extinction, stragglers held on in fresh water.
Synapomorphies:
- Dorsal fins confluent, with second fins spine lost
- The anterior dorsal fin spine is dissociated from the dorsal fin.
- Tail is, effectively diphycercal. The lower lobe appears as a second anal fin.
- Teeth are cladodont but forked, with the medial cusp reduced.
- Pectoral fin:
- Basals develop into an elongate metapterygial axis
- Radials on medial and lateral sides of metapterygial axis
Noteworthy plesiomorphy:
- The lateral otic fissure of the neurocranium persists. (In other elasmobranchs, it is closed.)
- Palatoquadrate suspension remains amphistylic.
Ctenacanthus from Oceans of Kansas
Synapomorphies:
- Fin spines with distinct characteristic ornamentation.
- The anterior dorsal spine slopes strongly posteriorly.
Hybodus sp. model at American Museum of Natural History
Synapomorphies:
- Characteristic fin spines.
- Hooked denticles on face.
White-tipped reef shark Triaenodon obesus
Synapomorphies:
- Placoid scales with:
- an outer layer of dense, enamel-like vitrodentin
- an basal collar of bone.
- Three distinct layers of tooth enamel.
- Hyostylic palatoquadrate suspension. Only a flexible ethmoid articulation remains. Enables protrusion of jaws to facilitate bite.
- Ethmoid region of braincase elongated into a rostrum that protrudes above mouth.
- Notochord calcifies into centra that correspond to neural arches. (Link to model)
- Pectoral and pelvic girdle elements articulate at midline.
Shortfin Mako Shark Isurus oxyrinchus by Callaghan Fritz-Cope
from Pelagic Shark Research Foundation
Galeomorpha also includes the large living suspension-feeding whale sharks and basking sharks, and the Cretaceous manta-ray mimic Aquilolamna milarcae (Vullo et al., 2021).
Synapomorphies:
- Expanded pharyngeobranchials
- Coracoids fully fused on midline
- Spiracle reduced or absent
Spiny dogfish Squalus acanthias from Wikipedia
Synapomorphies:
- Orbitostylic jaw suspension - palatoquadrate articulates to neurocranium via hyoid arch and orbital process of palatoquadrate
- Loss of anal fin
- Enlarged spiracle
- Addition of sixth or even seventh gill arch (E.G. Notorhynchus cepedianus)
- Enlargement of pectoral fins for stabilization and propulsion on bottom.
Diversity includes:
- Squalomorpha - Relatively unspecialized five-gilled cold-water sharks like Squalus acanthias (right).
- Hypnosqualea - Specialized bottom dwellers and their derivatives
Common guitarfish Rhinobatos rhinobatos from Wikipedia
Protospinax annectens from Wikipedia
Hypnosqualean schematic from Palaeos
- Ventrolateral and anterolateral cartilages of the nasal capsule support anterior head or articulate to the skeleton of the pectoral fin.
- Palatoquadrate articulation with neurocranium is utterly hyostylic, with no suggestion of a direct articulation with the braincase, and extremely mobile.
- The hyoid arch is simplified by the loss of ceratohyals and basihyals.
- Spiracles are greatly enlarged and are important in breathing.
- The last basibranchial articulates with the scapulocoracoid, functionally linking breathing and swimming.
- Anterior arcualia and centra fused into synarcual.
- Basal cartilages of pectoral fin articulate separately with scapulocoracoid.
Diversity includes:
- Squatinidae - Angel sharks
- Pristophoridae - Saw sharks
- Batomorphii - Skates, rays, sawfish, electric rays
Conflict! Alas, the "hypnosqualea hypothesis" is based on morphology. Molecular analyses find Batomorphii to be the sister taxon of all other neoselachians. Yikes.
Euchondrocephali:
Euchondrocephali: (Devonian - Quaternary) Total group including living Chimaeriformes and and all taxa closer to them than to Elasmobranchii . Living members, the Chimaeriformes, are clearly distinct from Elasmobranchii, but as one goes back in time, the two groups become harder to distinguish.Synapomorphies are technically complex except for one:
- Enlarged orbits
Euchondrocephali diversity:
Denaea from Carroll, 1988.
- Anterior dorsal fin lost or, in males, developed as bizarre display structures
- Anal fin lost
- Pectoral fin with extremely long metapterygial axis posterior to basal cartilages
Cladoselachida: (Devonian) Including Cladoselache, the earliest well-known chondrichthyan, and similar forms. Cladoselache known chondrichthyan from numerous well preserved skeletons. Roughly half meter adult length. Superficially shark like, anatomically suited as fast pursuit predator with tall tail, narrow trunk, and finlets to reduce drag of tail base. Stomach contents can include fish swallowed tail first, euconodonts, and invertebrates. One odd feature is the reduction of the pelvic fins and absence of anal fins. Absolutely none are known with claspers. Secondarily lost, or are all known specimens female?
Helicoprion beesonovi from Wikipedia.
- Often with long rostrum, E.G. Ornithoprion.
- One dorsal fin lost (but which?)
- Anal fin lost
- Pelvic fins lost. (Or so it appears. Strange. Did they use claspers?)
Debeerius ellefseni from Fossil Fishes of Bear Gulch
- The familiar broad otic process of the palatoquadrate is lost
- the hyoid arch is not involved.
Holocephali:
(Devonian - Recent) Living Chimaeriformes and their closest relatives: Many develop dermal skull plates made of dentine. Generally speaking, holocephalians are slow moving and specialize on crushing hard-shelled organisms.
Synapomorphies:
- Holostylic palatoquadrate suspension, a derived "special case" of autodiastylic condition, in which the palatoquadrate actually fuses with the neurocranium.)
- Teeth specialized for crushing - often fusing into broad tooth plates.
- The anterior arcualia fuse into a synarcual.
- Spine of the first dorsal fin articulates with the synarcual
- Second dorsal fin has no spine.
A rogue' gallery of Holocephali:
Iniopterygiiformes: (Carboniferous) Proportionally similar to chimaeras except:
- just as some rays taken to subaqueous flight using their pectoral fins, these seem to have done the same.
- Their pectoral fins attach far up on the body wall.
- They frequently have extensive bony plates on their skulls.
- Although Chimaeriformes (the living Holocephali) are specialized for crushing hard-shelled prey, at least one iniopterygian, Iniopera, has been modeled as using suction-feeding. (Dearden et al., 2023.)
Helodus simplex by Ghedoghedo from Wikipedia
- Distinctive tooth plate pattern.
- Frequent presence of paired "bottle brush" spines on head
Menaspis armata from Paleopedia
- Four pairs of head spines (derived from labial cartilages?)
- Bony dermal plates of head comprised of cyclomorial scales.
Belantsea montana from Wikipedia
- Petal-shaped teeth
- Broad pectoral fins similar to those of skates coupled with a laterally compressed body.
Rhinochimaera pacifica from Smithsonian Tropical Research Institute
Chimaeriformes: The Euchondrocephalian Crown
(Carboniferous - Recent) Noteworthy characteristics of Chimaeriformes - the living group:
- Odd cartilages of face perform numerous functions.
- Branchial arches tucked beneath braincase and covered by a single gill cover.
- Hyoid arch has a pharyngeohyal dorsal to the hyomandibula (analogous to pharyngeobranchials of branchial arches.)
- Hyoid arch supports the gill cover and has no association with the palatoquadrate.
Stem chondrichthyans:
As we survey farther down the chondrichthyan tree, we find creatures that share chondrichthyan synapomorphies but increasingly share ancestral characters with other gnathostome groups. A sampling:
Ozarcus mapesae from Pradel et al. 2014.
- The pharyngeobranchials slope anteriorly in the manner of Osteichthyes.
- Accessory elements like those seen in Osteichthyes are present
Doliodus problematicus pectoral fin from Miller et al. 2003.
Pucapampella (Early Devonian) Known from two braincases, according to Maisey and Anderson, 2001, this animal clearly preserves a ventral cranial fissure, otherwise known only from osteichthyans.
A general pattern emerges in which, the farther down the chondrichthyan branch we push:
- The less clearly distinct animals become from osteichthyans
- The more placoderm-grade plesiomorphic features we recognize.
Climatius from Wikimedia.com
Acanthodii
(Late Ordovician - Permian)A final gnathostome group demands attention: Acanthodii (aka "spiny sharks.") Small animals (10 - 30 cm) characterized by:
- Fin spines on all fins. (In some, intermediate fin spines develop from the ancestral postbranchial fin-fold. Also, cf. Doliodus, above.)
- Characteristic small rhomboidal scales that grow by circumferential accretion to a primordium.
- Often lack teeth or, when they are present, lack evidence for regular replacement. Dearden and Giles, 2021 note that teeth in many acanthodians are fused to a dermal "dentigerous bone" lining Meckel's cartilage or palatoquadrate, and suggest that teeth evolved more than once among them.
- Anal fin supported by a spine (unique)
Climatius from Carroll, 1988
- Very heavy fin spines.
- Four pairs of intermediate spines between pectoral and pelvic fins.
- Multiple external gill slits, partially covered by a larger operculum. (Armored by branchiostegal rays.)
- anterior and posterior dorsal fin.
Acanthodes from Wikimedia.com
- very light fin spines
- one pair of intermediate spines
- Gills entirely covered by operculum.
- Anterior dorsal fin lost.
- Overall resembling a spiny version of the basal osteichthyan Cheirolepis
Difficulty: Generally speaking, one would expect that in an evolving monophyletic group, the more derived taxa would occur later in time than the more ancestral ones. This is called stratigraphic congruence. Acanthodians display the opposite pattern. The most freakishly spiny ones are also early.
Acanthodes neurocranium mandibular, and hyoid arches
- Placoderms are paraphyletic
- Acanthodians are paraphyletic, with:
- some (like Climatius) basal to Eugnathostomata
- some (like Acanthodes) closer to Osteichthyes
- some (like Kathemacanthus) closer to Chondrichthyes
- a body covered with a mosaic of small scales but no dermal bone plates
- a cartilagenous endoskeleton
Everyone was happy that the enigma had been resolved. But only until 2013.
The Source of All Disquiet
Then came Zhu et al. 2013, reporting on Entelognathus primordialis, a placoderm-like creature with extensive bony cranial and thoracic armor and:
- Osteichthyan - like dermal cranial elements: the premaxilla, dentary, and maxilla.
- Jaw adductor musculature on both the medial and lateral sides of the palatoquadrate.
Adding color to this pattern:
- Sahney and Wilson, 2001 discovered the described the remains of open endolymphatic ducts in the acanthodians Brochoadmones, Ischnacanthus, Lupopsyrus, and Tetanopsyrus - a feature shared with living chondrichthyans but not osteichthyans.
- Davis et al. 2012 redescribed the skull of Acanthodes - the most osteichthyan-like of acanthodians - and found it to be more chondrichthyan-like than previous describers had.
- Brazeau and de Winter, 2015 examine the skull of Acanthodes, revealing that it's hyomandibula articulates with the braincase ventrally to the jugular vein, as in chondrichthyans. In osteichthyes, this articulation either straddles the vein or is dorsal to it. We don't know which state is derived, but the similarity to living chondrichthyes is striking.
Gladbachus adentatus from Coats et al., 2018 - Gladbachus adentatus (Middle Devonian) Coates et al., 2018 describe the results of his CT scans of Gladbachus, an 80 cm, chondrichthyan without fin spines, noting:
- The shape of the neurocranium is reminiscent of that of placoderm-grade gnathostomes
- The hyoid arch, although involved in jaw suspension, is not strongly differentiated from adjacent branchial arches
- The shape of the palatoquadrate suggests that at least some of the adductor muscle mass passed medially to it, as in placoderms.
- In their phylogenetic analysis, Gladbachus is nested among acanthodian-grade chondrichthyans - a spineless spiny shark!
Shenacanthus vermiform from Zhu et al., 2022 Scale bar = 5 mm!
- Martin Brazeau, (2009) The braincase and jaws of a Devonian "acanthodian" and modern gnathostome origins. Nature 457, 305-308.
- Martin Brazeau and Valerie de Winter, (2015) The hyoid arch and braincase anatomy of Acanthodes support chondrichthyan affinity of 'acanthodians.' Proceedings of the Royal Society B 282: 20152210. http://dx.doi.org/10.1098/rspb.2015.2210.
- Coates, Michael (2013) Sharks and the deep origin of modern jawed vertebrates The Palaeontological Association 57th Annual Meeting Podcast.
- Michael I. Coates, Robert W. Gess, John A. Finarelli, Katharine E. Criswell, and Kristen Tietjen. 2017. A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes Nature 541, 208Ð211.
- Michael I. Coates, John A. Finarelli, Ivan J. Sansom, Plamen S. Andreev, Katharine E. Criswell, Kristen Tietjen, Mark L. Rivers, and Patrick J. La Riviere (2018) An early chondrichthyan and the evolutionary assembly of a shark body plan. Proceedings of the Royal Society B 285(1870).
- Davis, Samuel P., John A. Finarelli, Michael I. Coates (2012) Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 247-250.
- Richard P. Dearden and Sam Giles, (2021) Diverse stem-chondrichthyan oral structures and evidence for an independently acquired acanthodid dentition. Journal of Vertebrate Paleontology 21(4), 702 - 713.
- Richard P. Dearden, Anthony Herrel, and Alan Pradel, (2023) Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera. Proceedings of the National Academy of Sciences 120 (4) e2207854119.
- John Maisey and M. Eric Anderson, (2001) A primitive chondrichthyan braincase from the Early Devonian of South Africa. Royal Society Open Science 8: 210822. https://doi.org/10.1098/rsos.210822.
- Alan Pradel, Tafforeau P, Maisey JG, Janvier P (2011) A New Paleozoic Symmoriiformes (Chondrichthyes) from the Late Carboniferous of Kansas (USA) and Cladistic Analysis of Early Chondrichthyans. PLoS ONE 6(9): e24938. doi:10.1371/journal.pone.0024938.
- Alan Pradel, John G. Maisey, Paul Tafforeau, Royal Mapes and Jon Mallatt (2014) A New Paleozoic A Palaeozoic shark with osteichthyan-like branchial arches. Nature 509, 608-611.
- Sarda Sahney and Mark Wilson, (2001) Extrinsic labyrinth infillings imply open endolympahtic ducts in Lower Devonian osteostracans, acanthodians, and putative chondrichthyans. Journal of Vertebrate Paleontology 21(4), 660 - 669.
- Leif Tapanila, Jesse Pruitt, Alan Pradel, Cheryl Wilga, Jason Ramsay, Robert Schlader, Dominique Didier. 2013. Jaws for a spiral-tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion. Biology Letters 9, 20130057. http://dx.doi.org/10.1098/rsbl.2013.0057.
- Kate Trinajstic, Carina Marshall, John Long, Kat Bifield. 2007. Exceptional preservation of nerve and muscle tissues in Late Devonian placoderm fish and their evolutionary implications. Biology Letters 3(2).
- Romain Vullo, Eberhard Frey, Christina Ifrim, Margarito A. Gonzalez Gonzalez, Eva S. Stinnesbeck, Wolfgang Stinnesbeck. 2021. Manta-like planktivorous sharks in Late Cretaceous oceans. Science 371(6535): 1253-1256.
- Zhu, Min, Xiaobo Yu, Per Erik Ahlberg, Brian Choo, Jing Lu, Tuo Qiao, Qingming Qu, Wenjin Zhao, Liantao Jia, Henning Blom & You'an Zhu (2013) The braincase and jaws of a Devonian "acanthodian" and modern gnathostome origins Nature 502, 188Ð193.
- Min Zhu, Per Erik Ahlberg, Zhaohui Pan, Youan Zhu, Tuo Qiao, Wenjin Zhao, Liantao Jia, Jing Lu, 2016. A Silurian maxillate placoderm illuminates jaw evolution. Science 354(6310) 334-336.
- You-an Zhu, Qiang Li, Jing Lu, Yang Chen, Jianhua Wang, Zhikun Gai, Wenjin Zhao, Guangbiao Wei, Yilun Yu, Per E. Ahlberg and Min Zhu. The oldest complete jawed vertebrates from the early Silurian of China. Nature 609, 954Ð958.
- Martin Brazeau and Valerie de Winter, (2015) The hyoid arch and braincase anatomy of Acanthodes support chondrichthyan affinity of 'acanthodians.' Proceedings of the Royal Society B 282: 20152210. http://dx.doi.org/10.1098/rspb.2015.2210.