GEOL 431 Vertebrate Paleobiology

Spring Semester 2021

Fossil Jawless Vertebrates

Chengjiang and the Burgess Shale provide an early glimpse of the first craniate chordates - stem vertebrates.

Myllokunmingia and Haikouichthys: Chengjiang gives us the best picture picture of what the ancestral vertebrate might have looked like with Haikouichthys ercaicunensis (right - possibly junior synonym of Myllokunmingia fengjiaoa) (Shu et al., 1999) which seem to preserve:

• 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

These have been boldly interpreted as basal vertebrates, in which the paired cartilages are arcualia and the fin texture is from cartilaginous fin-rays; and conservatively viewed as stem craniates, with the paired cartilages being branchial elements and the fin-rays being preservation artifacts.

Metaspriggina: And from the Burgess shale, Conway-Morris and Caron, 2014 describe Metaspriggina walcotti (right). In this case, the presence of eucondont-like eyes and W-shaped myomeres is unambiguous. More interesting is the presence of a branchial skeleton in which the skeleton is:

• internal to the gills
• Each branchial arch has an upper and lower element

In both respects, Metaspriggina resembles jawed vertebrates more than lampreys. Which state is plesiomorphic? Right now, GORK.

Hints of unseen diversity - conodonts

Euconodonta: (Cambrian - Triassic) Since 1856, paleontologists have been aware of minute (0.1 - 0.5 mm.) fossils made of apatite (calcium phosphate), the same mineral as vertebrate bone and teeth.

• 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.
  Thus, the word "conodont" was used to refer to the elements, themselves. The unknown creatures that made them were called "conodont animals."

Conodonts came in four general shape classes (right) and were always found as disarticulated clasts in marine sediment. This situation led to the very reasonable but unsupported assumption that each type of element represented a different taxon.

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 structures 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.

In the 1960s clarification came by the discovery of articulated groups of conodonts. For the first time it became clear that these elements (or most of them) worked together as part of a conodont apparatus.

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.

The conodont animal: Briggs et al., 1983, described Clydagnathus, an Early Carboniferous age eel-shaped creature in which he noted:

• 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.
• Notochord
• A head a brain and two capsules for special senses, thought to be very large eyes and smaller otic capsules.

We now have an emerging consensus on what the "conodont animal," now the monophyletic group Euconodonta, looked like - a small, eel-shaped chordate.

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.

Goudemand et al. 2011 describe the well-preserved conodont apparatus of Novispathodus, concluding that it was protracted during feeding by a rod-and-pulley arrangement similar to that of lampreys and hagfish. It seems plausible that such an arrangement is plesiomorphic (ancestral) for craniates. Link to animation.

The vertebrate evolutionary pattern:

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 is illuminated by Sansom et al., 2010 and Miyashita et al., 2019. So, we start with a review of bony evolution as revealed in these studies.

Note: The taxa depicted fall into three broad categories:

• Basal boneless craniates (Myllokunmingia, Metaspriggina, etc.)
• Total group Cyclostomi (Including Euconodonta!)
• Total group Gnathostomata

Bones

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 vertebrates 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.

This material is secreted and maintained by living cells:

• 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.

Bony tissue can be:

• Acellular if the bone cells migrate away as the bone is laid down and not enclosed by it. Particularly dense acellular bone is dentin (aka "dentine"), 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?

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:

Total Group Cyclostomi

Pharygolepis from BIOL202 - Susquehanna University

Anaspida (Silurian), Euphanerops (Devonian), and Jamoytius (Silurian)

These form a clade in analysis of Miyashita et al., 2019. Illuminated by well-preserved Jamoytius and Euphanerops. These were cylindrical, vaguely lamprey-like creatures with varying amounts of acellular dermal bone plates, but without specialize mouthparts. They lack obvious adaptations to suspension feeding or to taking large prey. Deposit feeders? Many morphological details reinforce the photo-lamprey impression:

• Hypocercal tail
• Anywhere from six to thirty branchial (gill) openings (compared to seven for lamprey). These usually formed a posteroventrally slanting row. In exceptionally preserved specimens of Jamoytius and Euphanerops, gills are organized in pouches with external branchial cartilage, like in lamprey.
• Retain a single median nasohypophyseal opening and nasal capsule (again reminiscent of lampreys).

But other characters reminiscent of gnathostomes or possibly the ancestral vertebrate condition:

• Single anal fin
• Lateral fin folds: hagfish and lampreys have no suggestion of paired appendages. In Euphanerops, Jamoytius, and Anaspida, 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.
• In anaspids, there are, additionally, paired triangular spines in a vaguely "pectoral" position. (red)
• Hard tissue takes the form of acellular strap and plate-like scales. In Jaymoutius and Euphanerops, these only occur on the trunk, but in Anapsida they extend onto the head.

Potential synapomorphies with Gnathostomata: (Therefore of Crown Vertebrata)

• Dermal skeleton.
• Anal fin
• Paired fin folds

Clydagnathus cavusformis from Nobu Tamura

Euconodonta (Cambrian - Triassic)

According to the parsimony analysis of Miyashita et al., 2019, these are stem cyclostomes. Their Bayesian analysis placed them as stem hagfish. Either result is plausible.

Total Group Gnathostomata

Thelodonts from Wikimedia Commons

Thelodonti (Ordovician - Devonian)

Morphology:


• 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



Furcacauda from PaleoStories
Furcacaudaformes: (Silurian - Devonian) While most thelodonts were slightly flattened dorso-ventrally, this group is morphologically distinctive in being:
• 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.
Nevertheless, there is a cottage industry in identifying potential synapomorphies between sub-taxa within Thelodonti and other vertebrate groups. These will be noted below.

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.
Stay tuned. We will note additional landmarks in the appearance of proper teeth in later lectures.

Synapomorphies of Thelodonti and jawed-vertebrates:

• Dermal denticles with distinct root, crown, and pulp-cavity.
• Paired nasal capsules.



Sacabambaspis janvieri from Paleoexhibit by Nobu Tamura

Pteraspidomorphi

(Cambrian (assuming Anatolepis) minimally Ordovician- Devonian).

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:

• Armor
• A reservoir of calcium and phosphate for use by the animal's metabolism.
• A solid skeleton against which muscles can act.
Note: It was not an internal skeleton.


Astraspis desiderata Athena Review
By the Silurian, many Sacabambaspis - like creatures are known, E.G. Astraspis (right).

Morphology:


• 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:
  • Eyes
  • 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 Wikipedia
Heterostraci: The great majority of pteraspidomorph diversity consists of Heterostraci, such as Pteraspis right.

Their synapomorphy:

• All branchial openings are covered by single armor plates, so that there are only two excurrent gill openings.
The largest pteraspidomorphs approached 1.5 m.


Drepanaspis gemuendenensis Palaeos
Without a living analog, speculations about the ecology of these creatures is very limited. We note the following:

Feeding:

• 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 or deposit-feeding - filtering particulate matter. They may have lived like an armored version of ammocoetes (larval lampreys).



Athenaegis chattertoni from PaleoStories
Janvier, 1997 suggests that the tail structure of basal pteraspidomorphs like Athenaegis (right) resembles that of furcacaudate thelodonts sufficiently to be a possible synapomorphy, suggesting that pteraspidomorphs might be derived from within Thelodonti. (According to Pradel et al., 2007, the tail of the early pteraspidomorph Sacabambaspis was strongly hypocercal, however.)


Synapomorphy of Pteraspidomorphi and jawed-vertebrates:

• Plate-like dermal bone formed in part from the coalescence of odontodes.



Interpretation of thelodont Turinia pagei (Early Devonian)
by Donaghue and Smith, 2001 from Palaeos

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.
We now move on to creatures whose feeding apparatus definitely indicates different feeding strategies.


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 cross-section from Histology at Southern Illinois University
• 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 (remember?), amoeboid mesodermal connective tissue of the embryo. Cartilage bone makes its evolutionary debut in the skeleton of the braincase but is widespread in vertebral columns and the skeleton of the limbs of derived vertebrates.

  
  

  
  However cartilage bones in living vertebrates actually form in two ways:
  • 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.




Shuyu zhejiangensis Institute of
Vertebrate Paleontology and Paleoanthropology

Galeaspida:

Restricted to southern China and Indochina, then a separate continent. (Silurian - Devonian)

Morphology:


• large flat head shield enclosing a 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 pteraspidomorphs 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.
Overall, although the equipment is different, the life-style looks like that of pteraspidomorphs: Bottom dwelling suspension/deposit feeding. But galeaspids are the first vertebrates in which the nasal capsules are separated from the hypophyseal duct. (See Gai et al., 2011 for details.)

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 Palaeos

Osteostraci

(Silurian - Devonian): Endemic to Euramerica. Resemble galeaspids in having large horseshoe-shaped head shields that include an perichondrally ossified brain-case, but with major differences:

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.
Other characteristics:
• 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.
• 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
Osteostraci are both informative and misleading. Their well-ossified brain-cases enable us to know their anatomy as in no other fossil jawless vertebrate, but aspects of this anatomy are enigmatic:
• 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 (???)

More and better fossils, please.

Coping with history: You will surely encounter the obsolete term "ostracoderms" in the literature. This refers 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.