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BONE

     There are a number of different organisms on earth today which incorporate inorganic ions (such as calcium, silicon, and iron) into hard protective structures.  This process is known as biomineralization.  The earliest animal known to perform biomineralization was the Precambrian worm Cloudina.

cloudina

The modern marine bloodworm Glycera dibranchiata is unusual in that it synthesizes a copper based biomineral in its jaws (Lichtenegger, 2002).

     Bone and cartilage are connective tissues and, as such, they are composed of specialized cells, extracellular protein fibers, and a ground substance.  The ground substance of vertebrate cartilage is composed of the gel-like chondroitin sulfate.  Cartilage-like tissue is actually known from a variety of organisms including vertebrates, jellyfish, annelids (sabellid worms), snails, cephalopods, horseshoe crabs, and the imagos of locusts.   Cartilage and neural tissue share a number of characteristics.  Chondromucoid, in the matrix of cartilage, is similar to molecules found in certain sensory receptors.  The cartilage proteins type II collagen and aggregan are also found in the nervous system.  Molecules once thought to be specific to cartilage (such as the chondroitin sulfate proteoglycan) have been found in the nervous system and proteins thought to be specific to the nervous system (such as S-100 acidic protein) have been found in cartilage. (Hall, 1999).

     Originally, jawless fishes were thought to possess true cartilage and certain invertebrate tissues were either classified as chondroid if they were similar to cartilage or chordoid if they were similar to the tissue of the notochord.  Given that lamprey and hagfish cartilages are now known not to possess collagen as a major component, any definition which includes the skeletal tissues of jawless fish as true cartilage also includes a number of invertebrate cartilages.  Cartilage/cartilage-like tissue is known in cnidarians, annelids, arthropods, and mollusks (Robson, 1999).  The cartilage of squid does possess collagen and resembles the hyaline cartilage of vertebrates, although it is not the collagen II found in vertebrate hyaline cartilage.  A variety of collagenous and non-collagenous proteins are known from invertebrate cartilages (excluding type II collagen) which seem to have evolved separately in different lineages (Robson, 1999).  

     Both nonsulfated chondroitin and polysulfated chondroitin are known in invertebrates (such as squid and crabs).  Acorn worms possess a cartilage-like skeletal rod ventral to the stomachord in the head region (Benito, form Harrison 1997, p. 16).  Enteropneusts possess gill bars and a proboscis “skeleton” which has been described as being similar to cartilage. (Benito, form Harrison 1997, p. 34).  The pharynx of Amphioxus stretches for half the length of the body and contain 100-200 gill slits (depending on the species).  Each gill bar contains a skeletal rod for support composed of collagen and glycosaminoglycans. (Ruppert, from Harrison, 1997, p. 434).  There is disagreement over whether the material which composes the gill bars of hemichordates (acorn worms and enteropneusts) and lancelets should be classified as cartilage or simply as a tissue similar to cartilage.  The mucopolysaccharides of the Amphioxus skin and notochord, although different from craniates (including lamprey and hagfish), are more similar to vertebrates than to those of invertebrates (Anno, 1975).

     Cartilaginous fish are the most primitive animals which produce cartilage with collagen type II (and type I). Hyaline cartilage in most vertebrates possesses collagen II as its major protein with lesser amounts of collagen types VI, IX, XI, and XII. Lampreys possess cartilaginous arches above the notochord.  Although type II collagen exists in the notochord of lampreys and hagfish, it is not a major component of agnathan cartilage.  The major protein in lamprey cartilage is named lamprin, that of hagfish cartilage is named myxinin.   Lamprin is homologous to vertebrate elastin, insect chorion proteins, and spider silk proteins (Robson, 1999).  Hagfish possess two types of cartilage, one of which is not like any other known vertebrate cartilage (and is similar to cartilage-like tissues found in invertebrates) and the second of which possesses a unique protein myxinin.  The alveolar cartilage of hagfish is different from that of lampreys in the amount of intercellular matrix and characteristics of the perichondrium (Tsuneki, 1993).  Lampreys possess a similar protein similar to myxinin (called lamprin) in their cartilage which can compose up to half the dry weight of the cartilage (Wright, 1984).  In lampreys, there are dense cartilages in the region of the brain and the neural arches around the spinal cord.  A different type of cartilage, alveolar cartilage. is found in the branchial and nasal regions. 

The earliest craniate fossils from the Cambrian possess no skeletal material other than the cartilage of the pharyngeal arches (Shimeld, 2000).

Cartilage from the gill bar of a fish is depicted below.

cartilage

      Collagen is the most abundant protein in the human body.  It composes about a quarter of bone and can compose a similar or greater percentage of cartilage (depending on the type of cartilage). It is not unique to humans or vertebrates with skeletal systems, however.  Collagen is the major extracellular protein of all animals and is even found in the simplest animals. A number of invertebrates have collagen fibrils very similar to the type of collagen found in vertebrates; collagen fibrils are even known from cnidarians and sponges.  Sponge collagen is homologus to that of vertebrates.  Since sponges can contain both fibrillar and non-fibrillar collagens, the amplification of this gene family had begun in the early animals (Exposito, 1990).   Although collagen was once thought to exist only in animals, it has been found in fungi where it composed the fimbriae which function in cell to cell communication.   Animal cells can interact with fungal collagen in a way similar to the manner in which they interact with animal collagens (Celerin, 1996).   Collagen sequences may have functioned long before collagen was an extracellular protein.  Collagenous sequences are known from vertebrate proteins such as acetylcholinesterase, C1q (a complement protein), pulmonary surfactant apoprotein, several lectins, and type I macrophage scavenger receptor.  The bacteria Streptococcus pyogenes possesses a collagen-like sequence in enzyme hyaluronidase (Stern, 1992).

     Bone is not known until jawless fish in the fossil record, but its ground substance is primarily composed of calcium and phosphate salts.  Calcium and phosphate are important metabolic molecules in all groups of organisms and are commonly used in metazoan animals. (Carroll, p. 23). 

     Vertebrates depend on vitamin D and its receptor in order to absorb the calcium necessary for the synthesis of bone.  The nuclear receptor for vitamin D, VDR, activates gene transcription after binding to vitamin D.  Although its major functions in mammals include the absorption of calcium for skeletal formation and regulation of the hair cycle, vitamin D receptors are expressed in lampreys which lack both bones and hair.  Lampreys may use this gene to induce P450 enzymes (Whitfield, 2003).

     The proteins of vertebrate enamel are not expressed in any other parts of the body and their function is unique, even among other biomineralized tissues.  Amelogenin is the major protein in vertebrate enamel, composing 90% of the organic portion of enamel.  One of its exons (exon 2) is homologous to an exon of proteins found in protostomes (osteonectin) and deuterosotmes (SC1, hevin, and QR1).  Enamel definitely existed in Ordovician ostracoderms while its existence in Cambrian euconodonts and fish such as Anatolepis is less certain (Delgado, 2001).

     The secretory calcium-binding phosphoprotein family (SCPP) includes three proteins in enamel matrix (amelogenin, enamelin, and ameloblastin), five proteins involved in the formation of dentin and bone (dentin, sialophosphoprotein, dentin matrix acidic phosphoprotein 1, integrin-binding sialoprotein, matrix extracelullar phophoglycoprotein, and secreted phosphoprotein 1, caseins, and several salivary proteins.  Most of these genes are located on a cluster on chromosome 4q13 in humans.  This gene family seems to have arisen from the SPARC gene.  SPARC, which is expressed in fish bone and scales, may have been the first gene expressed in vertebrate mineralized tissue.  SPARC is expressed where the epithelium meets the connective tissue beneath in invertebrates and jawless fish (Kawasaki, 2004). 

    The most primitive forms of cartilage in lancelets and jawless fish does not involve collagen.   SPARC is only associated with collagenous skeletal tissues.  SPARCL1 gave rise to amelogenin, enamelin, and ameloblastin early in the history of gnathostomes (Kawasaki, 2004).

     The cells which compose the human skeletal system arise through multiple embryological mechanisms.  In vertebrates, the caudal end of the embryo does not develop in the same manner as the cranial portion.  The tail develops neural tissue, muscle, bone, and blood vessels from tailbud mesenchyme without ever dividing into three germ layers.  In the cranial portion of vertebrate embryos, ectoderm and endoderm are the primary germ layers which induce the two secondary germ layers, mesoderm and neural crest cells.   Much of the embryonic skeletal tissue is produced by mesoderm.  In the head, neural crest cells (rather than mesoderm) form much of the skull (Halll, 1999).

neural crest
     Neural crest cells were a vertebrate innovation.  Amphioxus lacks them and lampreys have them (the situation in hagfish is not yet clear).  While Amphioxus lacks neural crest cells, it expresses many of the important genes involved in the differentiation of vertebrate neural crest cells in the region of the junction between the neural plate and the non-neural ectoderm.  Thus it appears that vertebrate neural crest cells employed genes which were already present in vertebrate ancestors (Ahlberg, 20-5).

THREE COMPONENTS OF THE COMPOSITE VERTEBRATE SKULL

    Although the adult skull in higher vertebrates is one solid structure, it develops from three separate parts: the chondrocranium, the splanchnocranium, and the dermatocranium.  The splanchnocranium is the oldest of the three structures.  The splanchnocranium, or at least its precursor, exists in protochordates around gills forming supports for gill arches.  Although the splanchnocranium in vertebrates is a product of neural crest cells, true neural crest cells do not exist in protochordates.  The splanchnocranium supports the roof of the pharynx in jawless fish (Kardong, 2002). 

gill archesgill arches

     The second portion of the skull to evolve was the chondrocranium and all craniates possess a chondrocranium under their brain (Kardong, 2002,  p. 233, 239). The chondrochranium and splanchnocranium compose the head skeleton of jawless fish and cartilaginous fish.  The head of lampreys consists of a number of cartilaginous structures and includes studs on the dorsal cranium similar to those observed in some fossil sharks and a pair of plates proceeding caudally from the occipital region (Dean, 1900).  In higher vertebrates, the chondrocranium and splanchnocranium serve as embryonic scaffolding for the development of the structures of the head and throat.  Some parts ossify and contribute to the bony adult skull.  In the shark skull below, the splanchnocranium forms the upper jaw (palatoquadrate), lower jaw (Meckel’s cartilage), and a series of branchial arches (including the hyomandibula of the second arch).  Obviously the gill arches are lost in adult amniotes, but the embryonic splanchnocranium contributes to the malleus (Meckel’s cartilage), incus (palatoquadrate), alisphenoid (palatoquadrate), stapes (hyomandibula of arch II), the hyoid bone (ceratohyal and basihyal components of arch II and the epibranchial, ceratobranchial, and hypobranchial portions of arch III), and larynx (derivatives of arches IV and V).  The embryology of the skeletal and muscular structures of the jaws suggest that jaws developed evolved from a modified pair of gill arches (arch I) (Kardong, 2002, p. 237)

chondrocraniumchondrocranium

chondrocraniumchondrocranium

shark skull

shark skull

shark skull
shark skull shark skull
The early gnathostomes evolved cartilage to form the orbital region, nasal capsules, ethmoid region, and an otic capsule around inner ear.  Parachordal cartilage and trabeculae from around notochord contribute in development of braincase (Romer, p. 192).  In humans, the chondrocranium contributes to the occipital bone (supraoccipital, exoccipital, and basioccipital regions), ethmoid bone (mesethmoid and turbinals), sphenoid bone (prespheniod, orbitosphenoid, and basispheniod regions), and temporal bone (petrosal and mastoid process). 

     Early jawless and jawed fish developed dermal bone as head armor, forming the third portion of the skull, the dermatocranium.  Dermal bone in the developing human embryo will form the following bones in humans: premaxilla, maxilla, nasal, lacrimal, zygomatic, squamosal (part of temporal), frontal, parietal, vomer, palatine, pterygoid, paraspheniod (the previous 2 forming parts of the sphenoid), and dentary.  Placental mammals have lost many of the dermal bones present in more primitive vertebrates such as the prefrontal, postfrontal, postorbital, intertemporal, supratemporal, tabular, quadratojugal, postparietal, ectopterygoid, splenials, angular, surangular, and a number of bones present in fish (such as the opercular series).

 

     Fossil jawless fish (such as the ostracoderms) and the primitive gnathostomes (placoderms) possess a dermatocranium composed of large plates of bone.  In the most primitive bony fish (acanthodians, pictured below) the dermatocranium is composed of many smaller bones whose patterns resembles that of higher fish although establishing precise homology is difficult (Carroll, p. 86). 

acanthodian  

After acanthodians the dermatocranium is more ossified and a pattern of dermal bones of the skull evolved which provided the basis of the dermatocrania of actinopterygians, sarcopterygians, and all tetrapods.  These higher vertebrates possess skulls composed of homologous bones (as indicated in the following images of a primitive actinopterygian, Cheirolepis, and a primitive sarcopterygian, Eusthenopteron ).

cheirolepis eusthenopteron
     In fossil jawless fish such as ostracoderms (such as that pictured below), bone existed in the skull while the rest of the skeleton was cartilaginous. 
jawless

Most vertebrates converted this postcranial cartilaginous skeleton (and cartilage in the skull as well) to bone. The same pattern is observed in higher vertebrate embryos, including those of humans.  In human embryos, bone is first laid down in the skull while the rest of the skeleton is cartilaginous.  Gradually this cartilage of the postcranial skeleton (and some in the skull as well) is converted to bone.

The human skeleton can be divided into two divisions: the axial division composed of the skull, vertebral column, and the thorax.

skeleton
THE CRANIUM

The Skull has two major regions: the cranium (which surrounds the brain) and the face.  (There are additional minor elements of the skull composed of the hyoid and the auditory ossicles).  The human cranium is composed of the frontal, parietal, occipital, temporal, sphenoid, and ethmoid bones.  The human  face is composed of maxillary, zygomatic, palatine, nasal, lacrimal, vomer, turbinate, and dentary bones.