Download Actinopterygians and Sarcopterygians

Biology 356 - Major Features of Vertebrate Evolution
Dr. Robert Reisz, University of Toronto
Actinopterygians and Sarcopterygians
Osteichthyes
Two major clades of osteichthyans are generally recognized, the
actinopterygians which appear in the Upper Silurian (isolated scales only) and
sarcopterygians appear in the Lower Devonian. Members of both clades are
generally active swimmers, and have a fusiform body.
The earliest known forms are marine, but they apparently spread rapidly into
brackish and freshwater environments. The available evidence indicates that
primitively, all had lungs, and the swim bladder of teleosts is a modified lung (and
is therefore homologous to the lung of tetrapods).
Actinopterygians
Their name means “ray-finned” because their fins are supported by several
endoskeletal rays and contain relatively little intrinsic musculature. This is an
extremely successful group of vertebrates, with a long history, and great
diversity. Actinopterygians are characterized by the presence of a single dorsal
fin, a caudal fin which primitively is fully heterocercal and deeply cleft. The
caudal fin is supported dorsally by epurals, distal to the neural arches, and by
specialized haemal arches called hypurals.
The earliest actinopterygians are collectively called palaeoniscoids or
chondrosteans. This is a paraphyletic group. The body is covered with small,
overlapping rhomboidal scales. Generally, the scales articulate with each other
by a dorsal peg that fits into a ventral socket of the scale above it. Each scale
consists of a basal layer of laminar bone, a middle layer of vascularized
dentine, and a superficial layer of enamel-like material called ganoine. The
scales grow by concentric addition of layers dorsally and ventrally. This type of
scale is called a ganoid scale. The notochord was probably unrestricted (this is
indicated by the lack of ossified centra) and extends to the tip of the tail. Paired
neural spines are found dorsal to the notochord and the posterior part of the
notochord also has haemal arches ventrally (See handout figures for early
actinopterygians). One or two additional rows of endochondral rods support the
dorsal, anal and caudal fins. These are the radials (located in the body, not in
the fin itself). There are also radials in the pectoral and pelvic fins, but these are
at the base of the fin, distal to the girdle.
The scales on the fins are narrow and longer than the body scales. They are
arranged in rows parallel to the orientation of the fin. These jointed scale rows
are called the dermal fin rays (lepidotrichia) and are primitively more numerous
than the endoskeletal rays (radials) that support them.
Their braincase has a narrow interorbital septum. The occipital plate is separated
from the otic capsule by the lateral cranial fissure. A ventral cranial fissure
separates the basioccipital from the basisphenoid. There was no mobility
between the elements separated by the fissures (unlike sarcopterygians, in which
the ventral cranial fissure allows mobility of the anterior half of the braincase).
Meckel’s cartilage is almost entirely surrounded by dermal bones, and is only
ossified as the articular. This small lower jaw element at the posterior end of the
jaw, forms a surface for articulation with the quadrate bone, an ossified element
of the palatoquadrate cartilage. The ossified element of the hyoid arch, the
hyomandibula articulates with the lateral commissure of the braincase
proximally, and with the quadrate distally, providing strong support for the jaw
articulation. There are four additional gill arches that are located posterior to the
hyoid arch.
The nasal capsules are small (poor olfaction). There is an incurrent and an
excurrent nasal opening (laterally). When the fish swims, water enters through
the incurrent (anterior) opening and exits through the excurrent opening. This
allows actinopterygians to smell the water in which they swim. The nasal cavity
does not communicate with the mouth.
In contrast to other Paleozoic fishes the skull elements seem to be homologous
with those of sarcopterygians and tetrapods. The dermal skull is divided into
functional units: the skull table (nasal, frontal, parietal, postfrontal, postorbital,
intertemporal), the cheek (jugal, quadratojugal, lacrimal, premaxilla, maxilla, the
opercular series (preopercular, opercular, subopercular) and the palate
(parasphenoid, pterygoid, palatine, vomer). See handout figures for these
structures in both groups of osteichthyans.
The dermal shoulder girdle supports the endochondral part of the girdle, the
scapulocoracoid, but it also serves as the insertion of the major hypaxial
muscles that open the mouth and expand the gill chamber. It includes the
clavicle, cleithrum, supracleithrum, posttemporal, lateral extrascapular and
medial extrascapular. The girdle extends from behind the skull table dorsally to
between the branchiostegal rays ventrally. Remember that the pectoral fin is
attached to the endochondral part of the shoulder girdle, the scapulocoracoid.
Actinopterygians have a special mechanism to open the mouth quickly. This
mechanism is useful for capturing prey. Actinopterygians use the a buccal pump
to create suction for breathing and to catch prey. Their epaxial muscles raise the
head, while the hypaxial muscles depress the lower jaw. At the same time, the
cheek moves laterally. This greatly expands the volume of the buccal cavity, thus
creating the suction. The branchial chamber can also be expanded, but it is used
mainly for breathing and usually doesn’t expand at the same time as the buccal
cavity. This helps create a continuous flow of water over the gills. Several
ichthyologists believe that this buccal pump which works with the
branchiostegal rays and the gular bones, is one of the major factors that
contributed to the great success of actinopterygians.
Neopterygians
In the Permian, some actinopterygians acquired several morphological
innovations and became very successful. These are called neopterygians, and
they include most modern actinopterygians (except for the extant taxa
Polypterus, acipenseriforms, and lepisosteids). They shared the following derived
characters:
The jaw adductor musculature appears to be larger, and the muscles extended
dorsally to the lateral wall of the braincase. This allowed for a greater gape for
more effective predatory action. The maxilla is separated from the cheek, freeing
it from the rest of the cheek, and there are relatively few teeth on this bone. A
joint appears between the maxilla and the premaxilla. It allows the back of the
maxilla to move ventrally and anteriorly. This allows to change the shape of the
mouth and helps in prey capture. The premaxilla becomes more elongate, with
most of the marginal teeth being attached to this bone. The overall effect is that
the jaws became shorter. Their articulation dropped below the level of the tooth
row, and a dorsally oriented process, called the coronoid process appears on
the dentary. All these changes greatly increase the strength of the bite. A new
element, the symplectic appeared between the vertical hyomandibula and the
palatoquadrate. This provides a stronger attachment of the jaws than a
hyomandibula alone. Reorganisation of the cheek region and of the opercular
series result in a more mobile skull (laterally). The cranial fissures close, but the
braincase is formed by more separate elements than in chondrosteans.
Posttemporal fossae develop to accommodate epaxial muscles.
The dentine layer of the scales was lost (only the basal laminar layer and the
enamel layer remained).
The number of dermal fin rays decreases and the scales of the fin rays fuse
(this results in stronger rays).
The caudal fin becomes not only abbreviated heterocercal, but even superficially
homocercal and the notochord no longer extends to the tip of the tail.
Intercalaries appear in the notochord (first rudimentary centra).
Uroneurals appear (specialized caudal neural arches; they are long and overlap
each other. They are paired rather than median).
Amia is one of the few living neopterygians that is not a teleost. Its history can be
traced back to the Upper Jurassic.
Teleosts
They are the most successful vertebrates. There are over 20 000 living
species. The fossil record of this clade is surprisingly long, with their first
appearance in the Late Triassic. List of autapomorphies include: The enamel of
the scales (ganoine) is lost. Only the basal layer of laminar bone remains. This
made the scales lighter and more flexible, allowing the fishes to swim better.
Completely ossified centra appear. The number of dermal fin rays decreases
further and matches the number of endochondral supports (radials). The caudal
fin becomes fully homocercal and the notochord is restricted to its base. Scales
in the region of the caudal fin sink beneath the surface and reinforce the base of
the tail. The pectoral fin has moved up to the area immediately behind the
operculum, and the pelvic fin has moved forward to a position nearly directly
beneath the pectoral fin. The dermal bones of the skull also lose the superficial
layer, allowing for the jaw musculature to attach to the outside of the skull.
Sarcopterygians
Traditionally, sarcopterygians have been divided in three main groups:
lungfishes, actinistians (coelacanths), and the rhipidistians (which form a
monophyletic group only if you include lungfishes and tetrapods in
them). Rhipidistians and coelacanths are sometimes classified together in the
Crossopterygii, but this taxon is also paraphyletic.
In strong contrast to the ray-finned fishes, sarcopterygians are characterized by
their unique fins structure, the massive fins being supported by a thick bony
endoskeleton that extends along the length of the fin. These skeletal elements of
the fin are supported by musculature that gives the fin its massive appearance.
Sarcopterygians differ from ray-finned fishes in having two dorsal fins. As in all
basal, early gnathostomes, the caudal fin is primitively heterocercal.
Their dermal scales also have a trilaminar configuration, with a basal layer of
laminar bone (isopedin), a vascular layer of bone, and a highly distinctive layer
of cosmine which has a very thin coating of enameloid material. It is because of
the presence of the cosmine, that these scales are called cosmoid. Primitively,
the scales were rhomboidal. Cosmine is a layer of dentine with a complex porecanal system that appears to have housed electrosensory organs. We think that
there was an electrosensory organ because the cavities and connecting canals
resemble the ampullary canals of Lorenzini of sharks and the ampullary and
tuberous organs of teleosts. This organ is especially useful in turbid water, where
it can locate prey better than the eyes. It is also a system that still seems to be in
use in the only living actinistian, the deep water marine Latimeria.
The traditional classification of sarcopterygians reflected overall similarities rather
than their phylogeny. The modern consensus on sarcopterygian phylogeny is as
shown here:
Modern consensus on sarcopterygian phylogeny. Notice that lungfishes are the
closest living relatives of tetrapods. Rhipidistians are a paraphyletic taxon.
Coelacanths (Actinistia):
They appear in the Middle Devonian. Primitively, they were marine and freshwater fishes, but by the Mesozoic they were mainly marine. This is the one of the
three groups of sarcopterygians that survive beyond the Paleozoic, the others
being tetrapods, and lungfishes. Although the above phylogeny places this group
at the base of the clade, this position is still controversial, and some specialists
consider them closer to tetrapods than the lungfishes.
Their lung lost its respiratory function early in the history of the group and
became calcified. Their braincase is divided into an anterior ethmoid unit and a
posterior otic-occipital unit. The division is created by a dorsal extension of the
ventral cranial fissure. The ethmoid unit could be depressed by a subcephalic
muscle. This produced a faster and stronger bite. Members of this group have
greatly reduced their marginal dentition. Surprisingly, there is no choana, only
two external nares. Diphycercal tail. The scales are cycloid and have no
cosmine. The nothochord is persistent throughout the group, with only tiny
central elements preserved. The body is short. Fleshy lobes are restricted to the
base of the fins, and the first dorsal is supported primarily by lepidotrichia that
often articulate directly with the basal. They acquired their modern appearance
by the Triassic.
There is no fossil record of coelacanths beyond the Cretaceous, at which time
they are known from shallow marine deposits. In 1938 the living coelacanth
Latimeria was discovered in the Indian Ocean near the island of Madagascar.
Porolepiforms and lungfishes:
Porolepiforms appear in the fossil record in the Lower Devonian. The members
of this group have no pineal opening and they have several tooth whorls lateral to
the symphysis rather than patches of small teeth or large fangs. Their bodies are
deep and short, and a relatively short skull. Porolepiforms share the following
derived characters with lungfishes: the posterior external naris is very close to
the edge of the mouth and the paired fins are very long and slender. The pectoral
fins are particularly elongate, and they attach to the pectoral girdle in a relatively
high position on the side of the fish.
Two of the best known forms are the Devonian forms Holoptrychius and
Porolepis. In general, this group is less well known than the other so-called
rhipidistians. One distinctive feature of members of this group is the presence of
two pairs of squamosal bones in the skull roof. The phylogenetic position of one
of the oldest known forms, Youngolepis from China is somewhat problematic, in
that it does not forms a clade with other porolepiformes, but rather is intermediate
between members of this clade and the lungfishes, possibly making the
porolepoformes paraphyletic. During the Carboniferours, porolepiforms became
large predators, one massive jaw indicating that its owner may have reached a
length of at least 6 m.
Lungfishes
They appear in the Lower Devonian. They are probably the closest living
relatives of tetrapods. They seem to be derived from porolepiforms. This implies
that porolepiforms as they are currently defined are a paraphyletic group.
Primitively, they lived in the oceans and in fresh water, but now they are found
exclusively in fresh waters.
Modern lungfishes retain lungs, and some will drown if prevented from breathing
air. Burrows from Permian and even the Devonian the indicate that aestivation
was possible early in the history of the group.
Their jaw musculature is very strong and spread medially over the
braincase. The palatoquadrate is fused to the braincase (holostylic jaw
suspension).
The dermal cranial bones are difficult to compare with those of other
osteichthyans; there is a different nomenclature for lungfishes. They have a large
opercular, but it may not be homologous to the bone of the same name in other
osteichthyans. Early lungfishes had a continuous layer of cosmine covering the
dermal skull bones. The only way that their skull could grow was to resorb the
cosmine, let the bones grow and redeposit the cosmine. There is evidence that
this happened seasonally.The palatal dentition is well developed and usually
forms tooth plates. The marginal dentition is absent. Premaxilla and maxilla have
disappeared.
Archipterygial paired fins (with radials on the preaxial and postaxial margins of
the main axis). This type of fin was once believed to be ancestral for
gnathostomes (this explains the name), but this theory has been abandoned.
There are no dermal shoulder girdle elements dorsal to the cleithrum.
Primitively, they had rhomboidal scales articulating with a dorsal process that
articulated with the next scale above. The centra were either crescentic or
cylindrical (but only one per segment in every case).
Ossified pleural ribs.
Diabolepis from the Lower Devonian of China is the most primitive lungfish. It
retained the following primitive characters: Mobile basicranial articulation.
Premaxilla is present and bears teeth.
The dentary retains marginal teeth. The teeth covering the pterygoid and
prearticular are densely packed and arranged in a radiating pattern, but they are
not fused into tooth plates.
Evolutionary trends in lungfishes: The oldest known lungfish already has the
specialized dentition that characterizes the group, creating a massive battery of
teeth on the pterygoid (palate) and the prearticular (mandible). In more advanced
forms these teeth fused into tooth plates, there is no tooth replacement, but
rather new teeth are added labially to the radial rows of teeth, and the old teeth
are retained lingually to form the tooth plate. Therefore, early tooth plates were
severely worn in old individual. Later, a pulp chamber developed between the
dentine of the denticles and the underlying spongy bone; wear of the dentine was
compensated by the continuous growth of dentine.
Other early dipnoans lose their teeth completely, and instead of teeth and plates,
have only denticles on their palate and mandible. Most of the middle and late
Devonian forms have well developed tooth plates with many radial rows of teeth.
One of the best know forms is Dipterus, in which much of the anatomy of the
animal is known. Later dipnoans are different from other osteichthyans in their
secondary reduction of ossification. Ossification of the endoskeleton was
reduced. After the Devonian, the snout, the braincase and centra were mostly
cartilaginous. The dermal bones of the skull became reduced in number and
size, lost their cosmine, and sank below the surface of the skin. The scales
became cycloid, lost their cosmine, and overlap extensively.
The lepidotrichia were replaced by horny camptotrichia (similar to the
ceratotrichia of sharks). The caudal fin became diphycercal (symmetrical), the
two dorsal fins and the anal fin moved posteriorly and became continuous with
the caudal fin. Lungfishes evolved fast in the Devonian, but very slowly after
that. They were essentially modern by the end of the Devonian.
Osteolepiforms:
They appear in the Lower Devonian. They became “extinct” in the oceans at the
end of the Lower Permian, after giving rise to tetrapods. They have the same
division of the braincase as porolepiformes, and the subcephalic muscles. The
dermal skull is similar to the skull of actinopterygians. The major differences are:
There is a hinge between the parietal and postparietal, above the joint in the
braincase. This is necessary to allow mobility of the ethmoid unit. The orbits are
smaller and the interorbital septum is wider. The nasal capsules are large and
well ossified. These features suggest that sarcopterygians relied more on
olfaction and less on vision than actinopterygians to capture their prey.
The bones around the pineal opening is called the parietal in rhipidistians, but it
is called frontal in actinopterygians. This is according to the prevailing
terminology in North America and most of Western Europe. However, it has been
repeatedly suggested that the bone bordering the pineal opening in rhipidistians
is homologous to the frontal in tetrapods. This theory seems to be supported by
the relationship between the lateral-line canal and the dermal bones of the
skull. This point of view is held by a small minority of scientists in Chekoslovakia
and Sweden. Most people call parietal the bone around the pineal opening (in
sarcopterygians). Around the orbit, there are prefrontal and postfrontal. On the
skull table, there are paired postparietals and tabulars. The quadratojugal is
large.
The sclerotic plate is composed of 30 sclerotic plates instead of 4.
In the palate, there is an internal naris (choana). There is a single paired
palatine, which bears large teeth. The vomer also has large teeth (rather than a
shagreen of denticles as in actinopterygians).
The lateral surface of the lower jaw is formed by a dentary dorsally and by
surangular, angular, postsplenial, and splenial ventrally. The medial surface is
covered by a prearticular and several coronoids.
As in many sarcopterygians, the enamel of the teeth are infolded. In crosssection, they look like a maze; this is why they are called labyrinthodont. This
infolding was retained in early tetrapods, and gave its name to a large group of
early “amphibians”.
The shoulder girdle includes more elements than in
actinopterygians. Sarcopterygians have an interclavicle, clavicle, cleithrum,
anocleithrum, supracleithrum, posttemporal, lateral extrascapular and medial
extrascapular (new elements in bold).
All have thin ossified centra. The shape of the centra varies considerably. Some
have cylindrical centra (eg. Megalichthys). Others have a paired, dorsal
pleurocentrum and a ventral intercentrum that may be paired throughout the
trunk but fused medially in the cervical and caudal regions (e.g.Osteolepis,
Eusthenopteron). This variability is especially annoying to paleontologists,
because this means that we don’t know which of these two patterns is primitive
for tetrapods.
The neural arches may be paired or median. In genera with cylindrical centra,
the arch articulates with the centrum, whereas the arches of genera with
crescentic centra are always separated from the centra by cartilage. There are
no zygapophyses. Genera with crescentic centra have ossified ribs, but genera
with cylindrical centra do not.
The base of the fins is covered by rhomboidal or rounded scales similar to those
covering the trunk. Distally, there are lepidotrichia. The caudal fin is supported
by neural and haemal arches, and epihaemal spines. The tail is primitively
heterocercal (Osteolepis), but some genera acquired a diphycercal tail
(Euthenopteron).
The endochondral elements of the paired fins can be homologized with those of
tetrapods. We can recognize the humerus, radius, ulna, the intermedium, and
ulnare in the forelimb. In the hindlimb, we can see the femur, tibia, fibula,
intermedium, and fibulare. The elbow and knee joints are already present, but
they may not have been as flexible as those of tetrapods. There are no
homologues of the distal tarsals, metapodials, and phalanges.
Homologies between rhipidistian and early tetrapod limb elements. The tetrapod
forelimb is based on Acanthostega. Its carpus is hypothetical and reconstructed
using Eryops. The hind limb is based on Ichthyostega. Some centralia were
added.
One group of osteolepiforms seems to be more closely related to tetrapods than
any other known rhipidistians. This is the Panderichthyida, known from the
Middle and Upper Devonian of North America and Eastern Europe. They share
the following derived characters with tetrapods (from Schultze and Arsenault,
1985, Table 1):
•
•
•
•
•
•
Skull broad and low (high and narrow in Osteolepis).
Orbits facing dorsally rather than laterally.
Pineal opening behind orbit rather than medial to it.
No intracranial joint (no hinge in the skull roof for kineticism).
Dermal scales and bones without cosmine.
No median fins, other than the caudal fin.
They are so similar to tetrapods that one of them had been thought to be a
tetrapod. However, they retain primitive, piscine characters lost in tetrapods,
such as:
•
•
•
•
Median gular plate.
Submandibulars.
Operculum.
Extrascapular.
Panderichthys is known from the Late Devonian of Latvia, shows that
characteristic streamlined body with long snout. The skull is markedly flattened.