HONR219d
Lecture 14
3-13-2012

The origin of Jaws and Gnathostome diversity

Gnathostomata: The jawed vertebrates. Quantum leap forward.

• Synapomorphies of hard tissues:
  • Branchial skeleton internal to gills. (In contrast to the external branchial basket of lampreys.)
    
  • The mandibular arch - i.e., the jaws, consisting of upper elements - the palatoquadrates and lower elements - Meckel's cartilages.
    
  • The hyoid arch, that helps connect the mandibular arch to the braincase.
    
  • Enlarged forebrain that is flexed ventrally with respect to hind brain. (Compare with ammocoetes larva of lamprey.)
    
  • Pharyngeal calcifications involving endodermal interaction with neural crest ectoderm - i.e. phayrngeal teeth.
    
  • Paired pelvic appendages
    
  • Horizontal (third) semicircular canal

Jaw anatomy: Up until now, when we have spoken of a "skull" we have meant only a plating of dermal bone around the head, or, in the case of Galeaspids and Osteostraci, that plus in endochondrally ossified neurocranium or braincase. With the appearance of the gnathostome jaws and branchial skeleton, the skull becomes a complex composite structure. The following illustrations show its components using the fossil bony fish Eusthenopteron as an example.

• Start with the neurocranium:

  
  

  

• Add the branchial arches:

  
  

  

• Add the hyoid arch:
  

  
  

  

• Add the mandibular arch - palatoquadrate and Meckel's cartilage:

  Note, whereas the branchial arches are separated from the hyoid arch and from one another by gill slits, the space between the hyoid and mandibular arches is either closed or perforated by the spiracle. (This is particularly conspicuous in rays, who breath in through it.) See also this link.
  

  

• Finally, add the dermal bone of the skull roof:

  
  

  

Origin of jaws: Many gnathostome synapomorphies are continuations of longstanding vertebrate trends toward increased skeletal ossification, brain enlargement, and improvement of swimming. Big exceptions are changes to the pharynx, especially jaws. We have:

• Jaws themselves - palatoquadrate and Meckel's cartilage.
  
• Internal branchial skeleton.
  
• Inductive formation of pharyngeal calcifications.

Oddly, fossil intermediaries between jawed and jawless vertebrates just don't seem to exist in the fossil record. What's up?

Four general hypotheses for this radical transformation:

• Gegenbaur's Serial homology:

  

  Carl Gegenbaur in 1870 proposed that the jaws and hyoid arch represented modified anterior branchial arches. In many modern gnathostomes, the jaws and hyoid arch enclose an opening called the spiracle (=eustacean tube in land verts) Originally, in Gegenbaur's scenario, they originally would have been separated by a complete gill slit. Gegenbaur predicted that fossil forms would be found with a complete gill slit between the mandibular and hyoid arches, but after a century of careful scrutiny, this has not happened. Ironically, Gegenbaur's hypothesis was so widely accepted that in some textbooks it is still treated as revealed wisdom.
  

• The New Mouth:

  
  

  Jon Mallatt, in the 1984, noted that the branchial arches of gnathostomes and lampreys can't be homologous, as they are medial to and lateral to the gills, respectively. (indeed, sharks retain extrabranchial cartilages lateral to their gills.) He agreed with Gegenbaur's opinion that the mandibular arch had originated as anterior (front) branchial arches. In 1996, he noted that although lampreys and fossil jawless vertebrates may lack jaws, they have cheeks and lips that enclose a large oral cavity. He proposed that the original mandibular arch had been behind the "old mouth," at the front of the pharynx, and had functioned in ventilation of the gills and sucking in prey. As the jaws became specialized for feeding, they moved forward, crowding the "old mouth" into the small space between the jaws and lips, and creating a "new mouth" - the oral cavity between the jaws and pharynx. The connection between breathing and feeding came from the use of the pharynx in suction feeding. Starting with the arches having had a secondary food manipulation function, they became specialized as primary feeding structures. This tied up one loose end, the presence of labial cartilages in sharks. Still, paleontological evidence of the transition has not been forthcoming.
  

• The Velar skeleton:

  
  But even Branchiostoma has a large oral cavity that is separated from the pharynx by the velum. Lampreys preserve this arrangement, but their velum is supported and moved by paired skeletal elements. In 1996, Phillippe Janvier proposed that the skeleton of the velum was the precursor to the mandibular arch. Like jaws, the cartilagenous velar elements of lampreys have upper and lower segments articulating at a posteriorly facing hinge. Alas, here, too, paleontological evidence currently falls short, as it it not obvious that other jawless vertebrates had a velar skeleton. Of course, such a structure would be hard to preserve.
  

• Neomorphic jaws: Mid 1970s, Bobb Schaeffer of the American Museum of Natural History proposed that jaws were neomorphs, inductively derived from the interaction of the endoderm of the pharynx and neural crest ectodermal tissue when the downturn and expansion of the forebrain brought the pharyngeal endoderm and neural tube ectoderm into close proximity. This has the advantage of explaining the absence of intermediate forms and the simultaneity of the appearance of jaws and the increase in brain size. Could this be associated with yet another hox gene duplication? All gnathostomes have four Hox gene clusters - one more cluster than lampreys (Hagfish may have experienced non-homologous Hox gene duplications, so theirs are hard to count).
  

Gnathostome diversity:

The orthodox "textbook" version is that there are major groups forming a polytomy:

• Placodermi (like Coccosteus below.)
• Chondrichthyes
• Osteichthyes

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"Placodermi": Silurian to Devonian armored gnathostomes experienced a rapid worldwide diversification and sudden decline.

• Synapomorphies:
  
  1. Distinct cranial and thoracic armor with unique ossification pattern.
     
  2. Jaws lined with self-sharpening occluding bony plates. (Whether or not these represent fused teeth is open to debate. Some placoderms, at least, had proper teeth.)
     
  3. Adductor muscles (that close the jaw) pass medial to (inside) palatoquadrate.

Placoderms were very diverse and occupied a wide range of ecological roles. Their specializations included:

• Shellfish feeding with crushing dental plates.
  
• Bottom feeding.
  
• Predation; Some of the largest predatory fish ever , such as Dunkleosteus, belonged to the placoderm group Arthrodira. The name refers to the proper joint at which their head and thoracic shields articulated. Many seem suited to resting on the bottom and engulfing prey by rapidly raising their head and opening jaws. Some localities, however, preserve streamlined pelagic (i.e. open ocean) placoderms.
  
• Some placoderms were detritus feeders. One group, Antiarchi, had greatly expanded box-shaped thoracic armor and pectoral fins enclosed in arthropod-like armor as well. Serial sectioning of some specimens suggests the possible presence of lungs. Perhaps the weird pectoral fins were used for crawling briefly on land?
• Some placoderms are known to have had sexually dimorphic an pelvic fins, suggesting that they practiced internal fertilization. In 2009 the fossil of a pregnant placoderm confirmed this.
  

Fossil record: Fragmentary records of placoderms appear in the Middle Silurian. this is followed by a rapid diversification. During the Devonian, placoderms were the dominant vertebrate group. Both marine and fresh water forms are recorded with a worldwide distribution except for puzzling absence in South American sediments. Placoderm diversity was greatly reduced by an extinction event in the Late Devonian. They were completely extinguished by the mass extinction event at the end of the Devonian. Thus, entire radiation took up only about 50 million years, but while it lasted, it was spectacular.

What placoderms lacked:

The myomeres of living gnathostomes differ from those of lampreys and hagfish in that there myomeres are divided into upper and lower halves by a horizontal septum of connective tissue. Lampreys' are not. Recent work on placoderm fossils with soft tissue preservation show that the placoderms, like lampreys, lacked the horizontal septum. This feature, therefore, is a synapomorphy of the two remaining gnathostome groups: Chondrichthyes and Osteichthyes.

Placoderm surprise: Over the decades, numerous phylogenetic analyses have yielded radically different interpretations of placoderm phylogeny. These analyses may have differed in their:

• Outgroup selection
• Character list
• Selection of taxa

But they all assumed that Placodermi was monophyletic, so there was no need to include a wide variety of other basal gnathostomes in the analyses. In such an analysis, is it even possible to test whether placoderms were monophyletic or not.

Recently, Martin Brazeau has analyzed basal gnathostome phylogeny and found that placoderms are paraphyletic, with some groups, including the arthrodires being more closely related to living gnathostomes and others, including the antiarchs, being more basal.

Chondrichthyes - Cartilaginous fish (Silurian - Rec.)

Basic definitions:

• For our purposes, Chondrichthyes (cartilaginous fish) is defined as all organisms more closely related to modern sharks and chimaeras than to any other gnathostomes.

  
  

• Living chondrichthyan diversity include:

  Sampling of diversity:
  

  • Holocephali: Chimaeras and fossil relatives
    
  • Elasmobranchii: Shark-like chondrichthyans.

  
  
• Synapomorphy: It is often said that chondrichthyans are characterized by lack of internal bone. While true, it is not quite diagnostic. In fact, the unambiguous synapomorphy of Chondrichthyes is the presence of prismatic calcification of the cartilage. In contrast with bone, prismatic calcification takes the form of chains of tiny apatite crystals covering the surface of cartilage, likend 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. To recap:
  

Fossil Material: Chondrichthyans are among the oldest known gnathostomes, but their fossil record is poor because their bodies lack preservable hard parts that stay articulated when they die. Two notable exceptions:

• Teeth

• Scales - Skin denticles

  These structures are similar in histology (microstructure) and differ mostly in size. Teeth are generated in a conveyor belt of gum tissue which moves them into place, then causes them to be shed and replaced by the next member of their tooth family in line. Modern sharks do this very quickly, with individual teeth being functional for a few days or weeks. This ability has evolved slowly and earlier sharks grew and shed teeth at a lower rate.

Ecological specializations: Before discussing phylogeny, consider what body types reveal about an animal's mode of life. These are informal designations and do not refer to groups necessarily related by common ancestry.

• Bottom feeders:

  

  Creatures live on the bottom, in essence grazing on a food source that does not have to be hunted - Detritus or slow moving organsims. It helps to have a body that stays in place and doesn't get wafted away by the current, hence these creatures are often flat or have broad supports. Being flat also makes one cryptic.

  
  

• Ambush predators:

  

  Creatures that stalk prey until they are in close range, then pounce on it, or those that lurk, waiting for prey to blunder into biting range. Examples we have seen include some of the large predatory placoderms. These tend to be critters that can accelerate quickly but have low top speed. Among fish, typically use torso for propulsion. This results from a trade off between drag and acceleration. For maximum acceleration, it is best to push with as much of the body surface as possible. Thus ambush predators tend to have deep bodies and tails that are not terribly distinct from the torso.

  
  

• Pursuit predators:

  

  Creatures that move faster than their prey, overtake, and overpower it. Needn't accelerate quickly, but have high top speed. Among aquatic predators, typically the tail is tall and half-moon shaped, like a propeller blade. Drag from the torso is reduced by making its lateral profile narrow.

Phylogeny:

Basal chondrichthyans: The earliest unambiguous chondrichthyan remains are from the Early Silurian, but consist of isolates scales. We get a good idea of what a primitive chondrichthyan looked like from Cladoselache: (Devonian) Earliest known chondrichthyan from numerous well preserved skeletons. Roughly half meter adult length. Superficially shark like, but hardly a proper modern shark.
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, conodont animals, and invertebrates. One odd feature is the reduction of the pelvic fins and absence of anal fins.

Chimaeras and kin:

• Holocephali: (Mississippian - Recent) Chimaeras and their relatives. Synapomorphies:
  
  • Palatoquadrate fused to braincase.
    
  • Teeth specialized for crushing - often fusing into broad tooth plates.
    
  • Branchial arches located beneath braincase and covered by a single gill cover.
    
  In addition, many holocephalians develop dermal skull plates made of dentine. Generally speaking, holocephalians are slow moving and specialize on crushing hard-shelled organisms.

  
  

• Both living holocephalians and their fossil relatives like Symmorida (Late Devonian - Pennsylvanian) had a tendency to develop sexually dimorphic display structures on their heads and anterior dorsal fins. Possible uses include:
  
  • courtship display.
    
  • structure by which the male actually grappled onto the female.
    

  • threat display structure.
    
  Note: Although Symmorids are superficially shark-like they are evidently closer relatives of Holocephali. Synapomorphy is that their lateral lines are protected by an armor of tiny calcified rings.

  
  
  

Elasmobranchii: (Devonian - Recent) Proper sharks and rays. Synapomorphy is a specialization of the branchial arches (don't ask). Earliest known elasmobranch is Antarctilamna from the Middle Devonian.

• Synapomorphy of Elasmobranchii and Holocephali: Pelvic claspers - modification of pelvic fins in males used as intromittant organs (i.e. to transfer sperm to females.) Ubiquitous in living chondrichthyans but not synapomorphy of group. Why not? Not seen in Cladoselache (maybe all our specimens are female but unlikely).
  

Note: Each dorsal fin has a fin spine (as in Port Jackson shark - right). Although these are prominent in sharks, they are probably plesiomorphich for chondrichthyes as a whole (or even for Gnathostomata?). Cladoselache has them, as do many non-chondrichthyan gnathostomes.

Like placoderms, elasmobranchs have occupied many ecological niches and embrace great diversity. Some interesting cases include:

• Fresh water predators of early Mesozoic.
  
• Skates and rays: Starting in the late Jurassic, bottom dwelling forms may have evolved independently more then once.
  
  • Morphology: Pectoral fins enlarged, In the most derived examples, such as stingrays, the skeleton of the forelimb articulates directly to the skull.
    
  • Defensive strategies:
    a. Stingrays line their posterior dorsal fin spines (located on the "tail" ancestrally the posterior torso) with toxins.
    b. Torpedo uses electric organs both to stun prey and to discourage predators.
    
  • Subaqueous flight: The marvel is that some, such as manta rays, cow rays, and eagle rays then took off of the sea floor and became secondarily adapted to subaqueous flight,

  
• Derived predatory sharks: Only in the Cretaceous do sharks begin to display their characteristic form with a long pointed snout, and lose their dorsal fin spines. At the same time, the ancestral anterior attachments of the palatoquadrate to the neurocranium are lost, allowing action of the hyoid arch to protrude the jaws from the head when prey is attacked.

Reproduction: Although all living elasmobranchs practice internal fertilization and produce relatively small numbers of large developed young, they display an amazing variety of reproductive strategies.

• Ovipary: Large, yolk-rich eggs are laid by some taxa. These are protected by egg cases, termed "mermaid's purse."
  
• Vivipary: Relatively large offspring born live. Embryos nourished by various means, including:
  
  • Pasta-like outgrowths of uterus eaten by offspring.
    
  • Infertile eggs shed into uterus and eaten by young.
    
  • Placenta, histologically similar to that of a placental mammal