The Origin and Evolution of Mammals - Moodle

114 THE ORIGIN AND EVOLUTION OF MAMMALS
the quadrate have been described earlier and the
functional significance of the implied changes in
size and orientation of the adductor jaw musculature
discussed. Establishing that two of the chain
of three mammalian ear ossicles (Fig. 4.9(a)), namely
the malleus and incus, are the homologues of the
respective reptilian jaw hinge bones, the articular
and the quadrate, and also that the mammalian
ectotympanic bone supporting the tympanic membrane
is the homologue of the reptilian angular
bone was one of the triumphs of pre-Darwinian
comparative anatomy (Reichert 1837). A satisfactory
functional explanation for the implied transition
from the one to the other took a little longer, in
fact not until 1975, when Allin’s hypothesis incorporated
several previously inexplicable details
(Allin 1975; Allin and Hopson 1992).
Apart from mammals, all living amniotes that
possess a tympanic membrane for air-borne hearing
transmit the vibrations of the membrane to the
fenestra ovalis in the otic capsule, and thus to the
cochlea canal of the inner ear, by means of the stapes,
or columella auris bone. This middle ear apparatus
provides an impedance matching mechanism
whereby the low pressure of the air-borne sound
waves is amplified to the higher pressure necessary
for water-borne sound waves. The ideal level of
amplification of the pressure is about 200 times. In
lizards, birds, and crocodiles, it is achieved partly
by the high ratio of the area of the tympanic membrane
to that of the fenestra ovalis membrane, a
‘stiletto heel’ effect. There is also a lever effect by
which the amplitude of movement of the tympanic
membrane at the outer end of the stapes is geared
down, and therefore the pressure increased at the
inner end of the stapes where it contacts the fenestra
ovalis. Mammals have an analogous mechanism.
Again the tympanic membrane has a much
larger area than that of the fenestra ovalis, around
100 times. A lever effect also exists, but it is completely
different and involves the chain of three
middle ear ossicles: malleus, incus, and stapes
(Fig. 4.9(b)). The big problem to understanding the
origin of mammalian hearing was always how the
reduced jaw hinge bones became interpolated
between a presumed functioning tympanic membrane
and stapes, of reptilian design. It is also true
that the acuity of sound perception in modern
reptiles and birds can be just as high as in mammals,
and therefore there seemed no apparent reason
to shift from one design to the other. Allin’s
(1975) proposal, not entirely new in principle but
for the first time convincingly argued, was that
tympanic sound reception evolved independently
in mammals from other amniotes, and that the
mammalian version of a tympanic membrane
originated from superficial tissues overlying
the postdentary bones in a pre-mammalian stage
(Fig. 4.9(c)–(g)). It was held largely by the angular
bone and its reflected lamina, which is the homologue
of the mammalian ectotympanic bone that
supports the modern mammalian tympanic membrane.
It also received some support at the back of
the jaw from the articular, which in turn articulated
with the quadrate of the upper jaw as the functional
jaw hinge. The quadrate itself made contact with
the external end of the stapes, and at the end of the
chain the inner end of the stapes was inserted into
the fenestra ovalis. In other words, the anatomical
relationships of tympanum, postdentary bones,
quadrate, and stapes in pre-mammals were the
same as in modern mammals. Allin’s proposal,
then, is that at some mammal-like reptile stage, a
crude form of tympanic-activated hearing already
occurred, no doubt limited to detection of lowfrequency
and high-amplitude sound. Subsequent
evolutionary reduction of the postdentary bones
and quadrate through the cynodont stages caused a
decrease in the inertia and therefore an increase in
the sensitivity of the system, a process which finally
culminated in the full mammalian system where,
once the new dentary-squamosal jaw hinge had
evolved, contact between the angular, articular, and
quadrate with the lower jaw was lost altogether.
Many features of cynodont jaw evolution support
this theory. The reorientation of the jaw muscles
to reduce the stress on the jaw articulation not
only increased the bite force at the teeth, but also
had the effect of allowing reduction in size and
increase in mobility of the hinge bones. On top of
this, Crompton (1972b) demonstrated that long
before the new dentary–squamosal joint evolved in
mammals, it was preceded in cynodonts by a secondary
contact between the surangular bone of the
lower jaw and a lateral flange of the squamosal. The
effect of this would have been to reduce the stress