Euconodonta and Jawless Vertebrates
Hints of unseen diversity - conodonts
- Highly diverse and rapidly evolving, thus excellent index fossils.
- Originally proposed to be the teeth of some unknown fish, but paleontologists soon determined they were were clueless about:
- What kind of animal they were from
- What part of the animal they represented.
At this point, speculation raged about:
- Which major taxon the elements belonged to
- How were they used? Originally proposed to be dental elements of fish-like chordates by Pander (1856), but soon, more erudite-sounding hypotheses held sway.
- To some they seemed likely to be used in prey capture, as in similar sturctures in chaetognaths (arrow-worms)
- To others, they seemed like mineralizations of the suspension feeding apparatus of cephalochordates.
- Or perhaps they were for internal support and not for feeding at all.
Moreover, different elements began to be distinguished by the manner in which they were formed developmentally.
Since these seemed to appear in a stratigraphic (chronological) sequence, speculation was that these growth forms represented evolutionary stages. Not quite. In 1988, single cone elements were eliminated from the roster of euconodonts by the discovery that they were the fossils of early chaetognaths. In living chaetognaths, similar elements are made of calcium carbonate and are used in prey capture.
- Chordate-like V-shaped segmented muscle blocks
- Midline fins supported by fin rays
- The conodont apparatus in an anterior position, suitable for use in feeding.
- A head a brain and two capsules for special senses, thought to be very large eyes and smaller otic capsules.
But where does Euconodonta go on the chordate cladogram? The presence of phosphatic hard parts arguably places it, closer to Gnathostomata than to hagfish or lampreys, but there are concerns:
- The conodont elements, as elements, are not homologous to any other phosphatic vertebrate feature.
- Jawless vertebrates might have secondarily lost hard tissues as a reversal.
- Some morphological interpretations of euconodonts, especially the huge eyes, seem to cry out for revision.
- The assumption of euconodont monophyly hasn't really been rigorously tested.
The earliest vertebrates:Chengjiang and the Burgess Shale have provided other records of basal vertebrates lacking conodont elements.
Haikouichthys ercaicunensis from Absolute China Tours
- W-shaped myomeres
- placode-derived special sense organs
- a branchial skeleton resembling that of lampreys
- Dorsal fin, with anteriorly sloping linear texture.
- paired cartilaginous elements near the anterior notochord
Metaspriggina walcotti from Science News
- internal to the gills
- Each branchial arch has an upper and lower element
We have such a copious record of heavily armored Early Paleozoic forms that it is tempting to forget that the group's most basal members (like Myllokunmingia) essentially lacked hard tissues. Indeed, the early evolution of Vertebrata is marked by the diversification of bony tissues and their proliferation through the body. This pattern was recently illuminated by Sansom et al., 2010. (Synopsis at right.) So, we start with a review of bony evolution.
Hagfish and lampreys, as the only living jawless vertebrates, provide an interesting glimpse of early vertebrate evolution, however they lack the proper hard tissues by which we know the vast diversity of early vertebrates - bone.
Fossil vertbrates are mostly known from hard tissues - bone and teeth. Bone is composed of:
- A mineral component - made of calcium phosphate (i.e. the mineral hydroxyapatite).
- A protein component - made mostly of the fibrous protein collagen.
- Osteoblasts: Active cells that secrete bone's extracellular matrix
- Osteocytes: When osteoblasts become trapped inside the bony matrix, they become inactive osteocytes and function in maintenance. In both life stages, these cells extend long processes (extensions) through canals in the bone. Osteoblast/osteocytes may be derived from nerve cells, whose axons and dendrites are similar. (Note: The corresponding cells responsible for bony tissue in teeth are called:
- odontoblasts/odontocytes when they secrete dentin
- ameloblasts when they secrete enamel)
- Osteoclasts: play a major role in bone remodeling by removing bone. They resemble and might be derived from macrophages.
Acellular (left) and cellular (right) bone from Dean and Shahar, 2012
- Acellular if the bone cells migrate away as the bone is laid down and not enclosed by it. Particularly dense acellular bone is dentin, characteristic of teeth and placoid scales. Dentin is characterized by parallel dentin tubules housing processes of the retreating odontoblasts.
- Cellular if the bone cells are enclosed inside the bone (right).
What is its history?
The earliest known phosphatic hard tissues were acellular, and were tooth-like in being made of:
- Dentin: Dense acellular bone
- Enamel: Bony tissue made entirely of interlocking crystals of hydroxyapatite (i.e. lacking collagen).
Among living craniates, bone in any form only occurs among members of Vertebrata - craniates with vertebral elements protecting their spinal cords. What does the study of fossil organisms tell us about the distribution of bony tissue?
Anatolepis armor from University of Toronto, BIO356
A rogue's gallery of early Paleozoic vertebrates:
As we do this survey, be aware of these issues:
- The proliferation of bone in the body
- The rise of the diversity of types of bony tissue
- Changes in the feeding apparatus
- Changes in the organization of the nasal capsules, hypophysis, and nasohypophyseal duct.
- Appearance of fin-like structures
The earliest vertebrate hard tissues are small acellular elements: conodont elements, which show outer layers of enamel covering layers of dentin. Conodonts were not the only representation of craniate hard tissues in the Cambrian, however. Enigmatic, scale-like plates of bony armor called Anatolepis were also present. In this and similar creatures, histologically tooth-like denticles complete with enamel and dentin formed a composite superficial body armor.
Indeed, in many early vertebrates, there seems to have been little difference between teeth and scales, which took the form of little denticles with a pulp cavity, dentin, and enamel.
The most basal vertebrates, however, lacked any hard tissues (except for conodont elements.) A survey of early vertebrate evolution should focus on their acquisition:
Euphanerops longaevus from Christian Science Monitor
Euphanerops (Devonian right) and Jamoytius (Silurian)
The phylogeny of Sansom et al., 2010 was made possible by reexamination of the important early vertebrate Jamoytius, often previously cited as the ancestral vertebrate or close to Hyperoartia. It seems to represent the first appearance of hard tissue elements outside the mouth: W-shaped bony acellular scales - composites of dentin and enamel. Other characteristics:
- Hypocercal tail
- Single anal fin
- Elongate row of over twenty branchial (gill) openings (compared to seven for lamprey).
Branchial openings: In Sansom et al., 2010, Jamoytius is found to be the sister taxon of the similar but soft-bodied Euphanerops (right) , which has a branchial array of roughly thirty openings that extends almost to the anus. Janvier et al., 2006 equate Euphanerops with Endeiolepis, and describe exceptionally preserved specimens of each, concluding that Euphanerops' gills were organized in pouches like those of a lamprey.
Fin folds: hagfish and lampreys have no suggestion of paired appendages. In Euphanerops, however, a pair of long lateral pleats extend down the ventral margins of the animal's trunk. They contain neither cartilage nor muscle, but suggest a starting point for the evolution of paired appendages.
- Hard tissue in the form of acellular plate-like scales, reminiscent of those of Jaymoutius, however these extend onto the head.
- Body is a slightly laterally compressed cylinder with notochord supporting lower lobe of a hypocercal caudal fin.
- Eight - fifteen branchial (gill) openings are small and form a short, posteriorly slanting row, reminiscent of the gill openings of lampreys.
- Retain a single median nasohypophyseal opening and nasal capsule (again reminiscent of lampreys).
- While there are no paired fins, there are paired triangular spines in a vaguely "pectoral" position. (red)
- Paired ventral fin folds are evident, beginning just behind the gill openings. (green)
Overall, anaspids seem adapted for active swimming. Exactly how they ate is mysterious, but they lack obvious adptations to suspension feeding or to taking large prey.
Synapomorphy of Anaspida and Gnathostomata: Dermal skeleton of head.
Thelodonts from Wikimedia Commons
Thelodonti (Ordovician - Devonian)
- Odontodes Hard tissue entirely consists of small scales that usually disarticulate when the animal dies. These odontodes are distinctive, consisting of dense and porous dentin layers around a pulp cavity, like a vertebrate tooth (!). Note: from this point on the tree onward, vertebrates generally retain scales of this sort or their derivatives, regardless of any other kind of skeletal ossification they may have.
- In some cases, these tooth-like scales line the oral cavity and pharynx.
- No proper paired fins, but many taxa have paired anterior triangular "fin folds" without skeleton or muscle that appear dorsal to the presumed position of the gill openings.
- One dorsal and one anal fin
- Hypocercal caudal fin.
- Paired olfactory capsules (in contrast to the vertebrates we have considered so far)
- Some well-preserved specimens appear to show a sediment-filled stomach, suggesting that they were deposit feeders.
- A series of eight - nine branchial (gill) openings
Living chondrichthyans preserve a similar pattern of denticles.
Furcacauda from PaleoStories
- laterally compressed
- distinct stomach present (it's earliest appearance in fossil vertebrates)
- Forked tail with major dorsal and ventral lobes, each of which supports up to four intermediate lobes.
- Paired fin folds present behind and below the gill openings. (In contrast to other thelodonts. Note: At least one taxon Shielia taiti has both types of fin folds. Are the two fin-fold types homologous?)
Thelodont monophyly: Is not assured. Recent analyses have (nearly) supported monophyletic Thelodonti:
- Donaghue and Smith, 2001 found non-furcacaudiform thelodonts to be monophyletic, with the furcacaudiforms forming a paraphyletic assemblage.
- Wilson and Märss, 2004 Found Thelodonti to be monophletic with Furcacaudiformes to be a basal clade.
Teeth without jaws? In several thelodonts, internal and external odontodes are clearly preserved inside the mouth and pharynx as well as in the skin. Rücklin et al., 2011 describe the odontodes of Loganellia scotica in detail. At present, these "internal" odontodes are the earliest plausible manifestations of teeth, although debate rages about:
- Whether the internal odontodes of thelodonts are homologous to gnathostome teeth.
- Whether internal and external odontodes are homologous in structure and development.
Synapomorphies of Thelodonti and jawed-vertebrates:
- Dermal denticles with distinct root, crown, and pulp-cavity.
- Paired nasal capsules.
Sacabambaspis janvieri Centre Nationale de la Recherche Scientifique - Evolution
The earliest well-preserved vertebrate, the Ordovician form Sacabambaspis, ironically represents a more derived form of hard tissue, in which individual denticles are integrated into broad head-shield composite elements and joined to one another through dermal layers of aspidin, a composite of thelodont-like denticles, dentin, and acellular bone. These shields are the first vertebrate elements that are bone-like in outward structure. Their possible functions include:
- A reservoir of calcium and phosphate for use by the animal's metabolism.
- A solid skeleton against which muscles can act.
Astraspis desiderata History of Life, Richard Cowen, University of California, Davis
in the form of acellular dermal armor consisting of dentin and aspidin. There is no internal bone. We see:
- Two armor shields, one dorsal and one ventral.
- Armor plates covering each gill opening.
- The mouth is opened and closed by row of narrow parallel plates in the lower "lip."
- Heavy placoid scales on posterior half of body.
- The dorsal and ventral head shields carry impressions of internal structures including:
- Otic capsules with impressions of two sets of semicircular canals.
- Paired nasal capsules, but with no evidence of nostrils. The capsules might have communicated with a medial nasohypophyseal duct. (but see Galeaspida, below, for an alternative.)
- Branchial (gill) pouches with possible branchial arch elements external to the gills as in lampreys.
- Midline ventral groove that might house "rod-and-pulley" style lingual apparatus.
- Notochord invades lower lobe of the hypocercal tail.
- There is no suggestion of dorsal, anal, or paired fins.
Pteraspis stensioei History of Life, Richard Cowen, University of California, Davis
- All branchial openings are covered by single armor plates, so that there are only two excurrent gill openings.
Drepanaspis gemuendenensis Palaeos
- If the distribution of pharyngeal slits is any indicator, they had a substantial pharynx.
- They lacked jaws, or even the keratinous structures that hagfish and lampreys use to process food. The implication was that they were suspension oe deposit-feeding - filtering particulate matter. They may have lived like ammocoetes (larval lampreys).
Athenaegis chattertoni from PaleoStories
Synapomorphy of Pteraspidomorphi and jawed-vertebrates:
- Plate-like dermal bone.
Issue: Transformation of feeding mechanics:Remember the rod-and-pulley oral mechanism found in hagfish and lampreys, and inferred in euconodonts? Although the internal feeding apparatus of Jamoytius, Euphanerops, anaspids, thelodonts, and pteraspidomorphs is poorly know, so far, we have not surveyed any animal that could not possibly have had such a feeding mechanism:
- those of pteraspidomorphs would seem to have required some mechanism to open the plates of the lower lip by pushing them forward
- rare well-preserved thelodonts display a mid-line structure (interpreted at right as the "esophagus") that could indicate a rod-shaped cartilage (among other possibilities). On could envision these working in concert with denticles lining the mouth and pharynx.
Issue: True Bone:Before proceeding, a note: The cells that secrete and maintain hard tissue may be locked within it, yielding cellular bone. Seen in larger bony elements. Cellular bone forms in two ways:
- Dermal bone: Laid down as a two-dimensional membrane. (E.g. human cranial bones). Ancestrally these formed near the body surface, but in derived vertebrates, their derivatives may invade deeper parts of the body.
Endochondral bone cross-section from University of Oklahoma Health Sciences Center
Interactive Histology Atlas
- Cartilage bone: Three-dimensional bone that is preformed in cartilage. (E.g. human limb bones). The cartilage, in turn, is preformed by condensations of mesenchyme cells, amoeboid mesodermal connective tissue of the embryo. (Remember them?) Cartilage bone makes its evolutionary debut in the skeleton of the braincase but is widespread in vertebral columns and the skeleton of the limbs.
- Perichondral ossification: Bone formation begins at the perichondrium - the membrane surrounding the cartilage precursor.
- Endochondral ossification: Bone formation begins in the interior of the cartilage precursor.
Note: Among living vertebrates, both types of ossification occur in cartilage bone, so neontologists and human anatomists call cartilage bone "endochondral bone." Paleontologists must distinguish them, however, because perichondral ossification evolved first and many fossil vertebrates have perichondrally ossified bone without the endochondral component.
Dermal bone cross-section from Histology at Southern Illinois University
Shuyu zhejiangensis Institute of
Vertebrate Paleontology and Paleoanthropology
- large flat head shield enclosing an perichondral bone braincase. The head shield is a composite of the perichondral braincase and composite dermal bone like that of pteraspidomorphs, except that this is proper cellular dermal bone, not aspidin.
- Head shield encloses lateral-line system.
- large nasopharyngeal opening in upper front of head shield (presumably used for inspiration of respiratory water.) leads to:
- paired olfactory capsules
- hypophyseal duct
- mouth and pharynx.
- mouth is ventral
- the endocast (impression of the brain on the inner surfaces of the braincase) indicates the presence of a paired cerebellum. Note: hagfish and lampreys lack this, gnathostomes have it, and the fossils of pteraspidomrphs are ambiguous.
- Braincase encloses openings for sense organs:
- Orbits - the bony eye-sockets
- Pineal foramen - for the pineal eye.
- Pharynx is large with up to 45 pairs of gill openings, suggesting suspension feeding.
- The floor of the pharynx is made of distinct plates that could be moved to expand the pharyngeal cavity and draw in water. There is not evidence (or room) for a "rod-and-pulley" tongue mechanism.
- No consistent dorsal or anal fins.
- Caudal fin diphycercal or slightly hypocercal.
- No suggestion of paired fins.
Synapomorphy of Galeaspida and jawed-vertebrates:
- Cellular bone
- Perichondral bone in brain-case
- Nasal capsules separate from hypophyseal duct
- Paired cerebellum
- Non-hypocercal tail
Ateleaspis tesselata (Late Silurian) from The Fossil Fishes of Great Britain
Synapomorphies of Osteostraci:
- Head shield contains three large sensory fields (two laterally and one on the midline). Internal channels link these to the otic capsules.
- An odd ventral fin flap laps beneath the caudal fin. This might be a modified anal fin.
- The floor of the pharyngeal chamber is flexible, facilitating inspiration of water.
- The oral and pharyngeal cavities seem to be separated by a velum.
- Posterior corners of the head can be drawn into cornual processes or "horns."
- Sclerotic ossicles support the sclera of the eyeball.
- Endolymphatic ducts connect the fluid filled labyrinth of the inner ear with the external environment. This is also observed in placoderm-grade gnathostomes and living Chondrichthyes. Link to example - scroll down.
- Notochord invades upper lobe of tail yielding heterocercal tail.
- One or two dorsal fins present
- Branchial openings slit-shaped. (Compare with lamprey)
- But the big thing: Paired pectoral fins (complete with calcified cartilage skeleton elements) present.
- Single median nasohypophyseal opening leads to a single olfactory capsule (like in lampreys) and to the hypophysis, and doesn't communicate with the pharynx - like the arrangement in lampreys.
Cephalaspis Bionet Skola
- What are the three "head fields?" Electric organs, elaborations of the lateral-line system, and outgrowths of the otic system are all suggested.
- Is the lamprey-like nasohypophyseal arrangement ancestral or secondarily derived? For decades, systematists linked osteostracans to lampreys because of it. Recently, the single nasal olfactory capsule and midline nasohypophyseal duct are considered to be a secondary reversal from a condition like that in galeaspids.
- Osteostraci share mesodentin with Katoporida, a thelodont taxon. Synapomorphy?
Synapomorphies of Osteostraci and jawed-vertebrates In any case, Osteostraci shares conspicuous synapomorphies with Gnathostomata:
- Endolymphatic ducts communicate with the exterior.
- Paired pectoral appendages with internal skeleton and muscle
- Heterocercal tail
- Two dorsal fins
- Sclerotic ossicles
- Slit-shaped branchial openings
Pituriaspis doylei and Neeyambaspis enigmaticaPaleoStories
Pituriaspida:(Devonian) A poorly known group with two known genera: Pituriaspis and Neeyambaspis from Queensland. Known only from their well-integrated, solid head shields. Generally similar to Osteostraci. Characterized by:
- An elongate rostrum (snout)
- Nasohypophyseal opening beneath shield in front of mouth.
- Mouth and pharynx organized as in Osteostraci
- Paired openings of unknown function beneath orbits (eye sockets)
- Opening for pectoral fins present in head shield
- Head shield extends far posteriorly. Possibly (?) forming support for pelvic appendage (???)
Coping with history: You will encounter the term ostracoderms in the literature. This referred to the vast paraphyletic grade-group of armored jawless vertebrates whose diversity we have surveyed.
Major Outstanding Issues:
- The position of soft-bodied craniates like Myllokunmingia and Metaspriggina
- The origin and homology of paired fins
- Thelodonts - monophyletic or paraphyletic?
- The evolution of the organization of the head (braincase, nasohypophyseal duct, nasal capsules, etc.) in vertebrates lacking cartilage bone.
- The evolution of the weird nasohypophyseal duct of Osteostraci.
- Derek Briggs, Euan Clarkson, and Richard Aldridge. 1983, The Conodont Animal. Lethaea, 16(1), 1-14.
- Simon Conway Morris and Jean-Bernard Caron. 2014. A primitive fish from the Cambrian of North America. 512, 419-422.
- Mason Dean and Ron Shahar, 2012. The structure-mechanics relationship and the response to load of the acellular bone of neoteleost fish: A review. Journal of Applied Ichthyology, Feb.
- Philip Donoghue and M Paul Smith, 2001.The anatomy of Turinia pagei (Powrie), and the phylogenetic status of the Thelodonti. Transactions of the Royal Society Edinburgh, Earth Sciences. 92: 15-37.
- Philip C. J. Donoghue and Joseph N. Keating. 2014. Early vertebrate evolution. Palaeontology. Early View online version August 16, 2014.
- Zhikun Gai, Philip Donogue, Min Zhu, Philippe Janvier, and Marco Stampanoni. 2011, Fossil jawless fish from China foreshadows jawed vertebrate anatomy. Nature, 476, 324-327.
- Nicolas Goudemand, Machael Orchard, Severine Urdy, Hugo Bucher, and Paul Tafforeau. 2011, Synchrotron-aided reconstruction of the conodont feeding apparatus and implications for the mouth of the first vertebrates. Proceedings of the National Academy of Sciences, 108(21), 8720-8724.
- Philippe Janvier. 1993. Patterns of diversity in the skull of jawless fishes. In The Skull (ed. J. Hanken and B. K. Hall), Vol. 2, pp. 131 - 188. The University of Chicago Press.
- Philippe Janvier. 1997. Thelodonti. In The Tree of Life web site, http://tolweb.org/tree?group=Thelodonti&contgroup=Vertebrata, recovered 12/29/2015.
- Philippe Janvier. 2006. Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate. Nature 440, 1183-1185.
- Philippe Janvier. 2007. Homologies and Evolutionary Transitions in Early Vertebrate History. In Major Transitions in Vertebrate Evolution. (eds. Hans-Dieter Sues and Jason Anderson), pp. 57 - 121 Indiana University Press, Bloomington.
- Tiiu Märss and A Ritchie (1998), Articulated thelodonts (Agnatha) of Scotland, Transactions of the Royal Society Edinburgh, Earth Sciences. 88: 143-195.
- Pander, Heinz. 1856. Monographie der Fossilen Fische des silurischen Systems der Russisch-Baltischen Gouvernements (Monograph of fossil fish from the Silurian stratum of the Baltic regions), St. Petersburg
- Alan Pradel, Ivan. J Sansom, Pierre-Yves Gagnier, Ricardo Cespedes, Philippe Janvier. 2007. The tail of the Ordovician fish Sacabambaspis. Biology Letters 3(1).
- Martin Rücklin, Sam Giles, Philippe Janvier, and Philip Donoghue. 2011. Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evolution and Development 13(6) 523-532.
- Robert Sansom, Kim Freedman, Sarah Gabbott, Richard Aldridge, and Mark Purnell. 2010. Taphonomy and affinity of an enigmatic Silurian Vertebrate Jamoytius kirkwoodi White. Palaeontology 53(6), 1393-1409.
- D-G. Shu, H-L. Luo, S. Conway Morris, X-L. Zhang, S-X. Hu, L. Chen, J. Han1, M. Zhu, Y. Li, and L-Z. Chen. 1999. Lower Cambrian vertebrates from south China. Nature 402, 42-46.
- Mark Wilson and Tiiu Märss. 2009. Thelodont phylogeny revisited, with inclusion of key scale-based taxa. Estonian Journal of Earth Sciences. 58, 297-310.
- Simon Conway Morris and Jean-Bernard Caron. 2014. A primitive fish from the Cambrian of North America. 512, 419-422.