AM. ZOOLOGIST, 6:371-377(1966).
Evolution of the Sense of Hearing in Vertebrates
WlLLEM A. VAN BERGEIJK*
Bell Telephone Laboratories, Inc., Murray Hill, Neio Jersey
SYNOPSIS: This paper briefly recapitulates work on the preterrestrial phase of the evolution
oE hearing which was published in detail elsewhere. Following this, the problem of the
origin of the terrestrial middle ear is examined in some detail, and it is demonstrated that
Eusthenopteron, and probably other rhipidistians as well, possessed an eardrum. This drum
was formed by the fusion of the distal surface of a spiracular diverticulum and a ligament
between parietal shield and squamosal. It is further demonstrated that the geometry of
this eardrum in relation to the middle-ear cavity was adequate to allow the fish to make
the transition from aquatic hearing to terrestrial hearing without loss of sensitivity.
As the various papers presented in this paper of R. M. Denison in this Symposium),
Symposium demonstrate, the evolution of we pick up the thread of evolution at a
the ear as a morphological entity has been point where a hypothetical early vertebrate
intensively studied, and a considerable de- (or pre-vertebrate) had a functional lateralgree of understanding has been attained line system. We assume that this lateralis
with regard to the homologies of structure system remained, as far as its functional
that exist. The same cannot be said of aspects arc concerned, essentially the same
the evolution of hearing as a physiological up to the present. Thus, we can bring to
phenomenon. The reasons for this state of bear the results of Cenozoic research on
affairs are obvious: morphological hypothe- Paleozoic problems. The lateral line (see
ses can be tested quite readily by examina- Dijkgraaf, 1963, and van Bergeijk, 1966, for
tion of fossil material, but hypotheses about extensive discussions) is a sensory system
function are virtually untestable, since that responds to water motions. It is not
physiology demands a living body for the sensitive to pressure or pressure waves, and
test. What information we do have about thus not to sound in the conventional sense.
the evolution of function is, therefore, However, a real sound source in water
based heavily on physical principles, morph- produces water motions as well as pressure
ological evidence, logical inference, and waves in its near field. These near-field
analogy with the known physiology of con- water motions excite the lateral line (Hartemporary species.
ris and van Bergeijk, 1962), and thus it
In a recent paper (van Bergeijk, 1966) can be said that the lateral line is sensitive
I proposed an outline for a theory on the to near-field sound. The old controversy of
evolution of hearing, which was based on whether the lateral line does or does not
just such a variety of sources. The present respond to sound is thus laid to rest by
paper will expand somewhat on that work; the simple expedient of denning "sound"
specifically the evolution of the terrestrial more accurately. Moreover, the lateral line
middle ear will be considered. In order is directionally sensitive (van Bergeijk,
to be properly understood, however, I must 1964), and enables the animal to locate a
briefly restate the salient points of my source of disturbance at a distance. One
can argue endlessly whether "distant touch"
earlier paper.
or "nearby hearing" is the more appropriate term to describe this sensory system;
PRETERRESTRIAL EVOLUTION1
the distinction so far is largely semantic,
Although the origin of the lateral line is since neither description leads to concluby no means a solved question (see the
• Present address: Center for Neural Sciences,
Indiana University, Bloomington, Indiana 47401.
1
In order to minimize clutter, only key references
will be given; I refer to my earlier paper for more
thorough discussion and further references.
(371)
372
WlLLEM A. VAN BERGEIJK
sions which the other does not also imply. Harris, 1964). As a result of the changes
Hearing in the conventional sense, viz., the in volume of the bladder, near-field waterperception of pressure waves, is not deriv- motions (as well as pressure waves) radiate
able directly from lateral-line perception from it. The inner ear is sufficiently close
anyway, since an additional structure (hav- to this source of near-field motions to being nothing to do with the lateral line) is come excited by them, and a new sensory
required for the transformation of pressure channel is opened: thanks to the pressureto water motion.
to-displacement transformer-action of the
But first came the inner ear, the laby- swimbladder, the inner ear is now sensitive
rinth. Initially, it had nothing to do with to pressure waves. It hears.
hearing, even near-field hearing. In fact,
Various adaptations evolved that appear
it appears that the labyrinth is a successful to increase the sensitivity of this new sensory
attempt to isolate part of the fluid-motion channel. The bladder becomes connected
detector-apparatus of the lateral line from to the inner ear by means of a chain of
outside disturbances, and put it to work ossicles (Weberian ossicles of Ostariophysi),
to detect movements of the animal's own bladder extensions (in clupeids, for exbody. The simple ears of Myxine and ample), or other specializations. The effect
Petromyzon, for instance, make sense as of such connections is primarily to minimize
angular and linear accelerometer systems, transmission loss, though some equalization
and the evolution from one to two to three of frequency and acoustic filtering are possemicircular canals is a very nice example sibly important secondary functions. Data
of increasing precision in a biological available in the literature (see van Bergeijk,
measuring device.2 By being sunk deeply 1966, for discussion) appear to support
into the skull, the inner ear is much less these notions. The inner ear evolves specialsensitive to near-field motions in the ex- ized sensory sites that deal exclusively with
ternal environment than the lateral line, fluid motions originating from the swimand it is, of course, certainly not more bladder, and contributes its part to a lowsensitive to pressure waves.
loss transmission path by the development
The structure that converts pressure vari- of a perilymphntic system.
ations into water motions is the swimbladThe pressure-sensitive ear of fishes is,
der. It can be regarded as essentially a gas however, not sensitive to the direction of
bubble, having a primary function for sound. Whereas the lateral line is capable
buoyancy perhaps, or respiration; the origi- of locating the source of near-field motions
nal function of the organ, or the selection quite accurately, the ear of fishes is inpressures to which it is (presumably) an capable of locating the source of a pressure
adaptation, do not concern us here. Being wave (van Bergeijk, 1964).
a gas bubble, a swimbladder will obey the
The swimbladder with its extensions or
gas laws and change volume when pressure
is changed. It will follow variations in ossicles may, quite properly, be considered
pressure over a considerable range of fre- a middle ear; its function and mode of
quencies because, although it has a definite action are the same as those of the terresresonance frequency, damping is so high trial middle ear, which also is essentially a
that the response curve is almost flat (see trapped air bubble, changing volume under
the influence of pressure waves. First, however,
we must examine the origin of the
s
I t is sometimes proposed that the myxinoid ear
is a degenerative version, rather than a primitive terrestrial middle-ear gas-bubble, for it is
one; this seems unlikely to me, for why should the clear that it does not derive from any sort
ear degenerate in an actively swimming hagfish of swimbladder. Instead, the middle ear
but remain beautifully intact in such an almost is derived from the first, or spiracular,
sedentary animal as a flatfish? Moreover, in degeneration it is size and differentiation that are pouch of the pharynx. There are some
modern, teleost, fishes, notably members of
reduced, not dimensionality.
EVOLUTION OF HEARING IN VERTEBRATES
the genus Ophicephalus (now, Channa),
which possess air-filled diverticula of the
spiracular pouch that serve as auxiliary
respiratory organs. Other modern fish, such
as the anabantids, have similar air-pouches
although these do not derive from the first,
but from one of the other gill pouches.
These air-filled sacs have been demonstrated
to be important for hearing in those fish
(Schneider, 1941).
Some Devonian Rhipidistia, notably Eusthenopteron, possessed diverticula of the
spiracle; some cogent arguments can be
made for (and none against) the assumption that this rhipidistian pouch also was
filled with air, and served as a middle ear
(van Bergeijk, 1966; see also K. S. Thomson's paper in this symposium). Thus, as
the earliest amphibians evolved from the
rhipidistians, the terrestrial middle-ear
cavity was already present morphologically
and was, as we shall see, apparently functional. Pharyngeal middle ears are distinctly superior to a swimbladder middle ear in
fish. For one thing, the air bubbles rest
almost directly against the inner ears, and
no special chains of ossicles are required
for efficient transmission; more importantly,
there are now two sound receptors which, at
least in principle, allow directional hearing
in the far field. The emergence on land,
however, poses some special problems for
this hearing apparatus which we shall now
examine in some detail.
EVOLUTION OF THE TERRESTRIAL MIDDLE EAR
The problems encountered by the rhipidistian hearing apparatus with the emergence on dry land are traceable to just one
factor: the acoustic impedance of air. Acoustic impedance for plane waves is given by
the product of density Q>) of the medium
and the velocity of sound (c) in the medium. The impedance of water (and, to a
first approximation, of living tissue), pcwater,
is about 153,000 g/cm2/sec (the exact
value depends on temperature, atmospheric
pressure, solutes, and other factors; the
value given is only intended as representative). The acoustic impedance of air
373
(pcair)> however, is only 39.5 g/cm2/sec»
or about 1/4000 that of water.
One important consequence of this difference is that a sound source in air produces
only 1/63 of the pressure3 developed by an
underwater source of the same intensity
(power transmitted/cm2). This ratio, conventionally expressed in decibels (in this
case, some 36 dB), represents the "hearing
loss" suffered by a rhipidistian that crawled
out of the water onto land. For the middle
ear is a pressure-sensitive device, and it is
the sound pressure that is diminished in
air as compared to water.4
This loss of sensitivity is, however, at
least partially, and perhaps largely, offset
by a peculiarity in the anatomy of the
spiracular diverticulum and the bones surrounding it. We shall take Eusthenopteron
as an example, because there is a great deal
of detailed information available about this
fish; whether other rhipidistians show similar structures is not known to me.
In Figure 1, redrawn from Jarvik (1954),
is shown part of the skull of Eusthenopteron. The dermal bones are removed (although some are shown in outline by a
heavy dashed line), and the palatoquadrate
is similarly left off. Thus the view is into
the medial wall of the spiracular diverticulum. The lightly dashed line, running
along the dorsal margin of the hyomandibular, outlines the dorsal extent of the removed half of the diverticulum. The diverticulum is a rather flat and broad one,
sandwiched as it were between the hyomandibular and parotic dental plates and the
palatoquadrate. According to Jarvik (op.
cit., p. 50) the diverticulum probably opens
to the outside along this cleft. If that
a
The ratio of pressures in air and water is proportional to the square root of the ratio of the
impedances.
4
We assume here that the power output of sound
sources is about equivalent in air and water, since
the power of a source is a function of the energy
available to it, as well as of the radiation impedance. For biological sources (mates, prey, predators) this is quite probably the case; if anything,
they are less efficient in air because of poorer
coupling, and thus the effective power of these
sources may be less in air than in water.
WrLLEM A. VAN BERfiEIJK
374
SPIRACULAR
PARIETAL
CANAL
INTERTEMPORAL
1
SUPRATEMPORAL
DIVERTICULUM - < -
SQUAMosAi
HYOMANDIBULAR
DENTAL PLATE
10MM
FIG. 1. Otic region ot the skull of Euslhenopteron. Palatoquadrate removed to show hyomandibular side of spiracular diverticulum. Heavy
dashed lines: outlines of dermal bones covering
the skull; names of these bones are underlined.
Redrawn from Jarvik (1954).
were true, then no air could be contained
in it, and it would act perhaps as an extra
spiracle. It seems, however, rather unlikely
that this is the case, because the spiracle
itself opens, via a separate canal, to the outside at the extreme front end of the cleft
(see Fig. 2). Why should a diverticulum
develop that is just a parallel channel to
an already existing one? Jarvik offers no
support for his statement and, in fact, makes
it essentially en passant; he appears to have
given it no further consideration.
Thomson (this symposium), on the other
hand, states that there must have been a
Jigamentous connection of the squamosal
with the bones of the parietal shield (supratemporal and postspiracular, 5 see Fig. 2, A),
because without such a ligament the skull
would have fallen apart. These dermal
bones overlie the hyomandibular and palatoquadrate, and the ligament between them
allows no place for the diverticulum to open
up to the surface. More significantly, as
shown in Figure 1, the margins of the dermal bones (supratemporal-postspiracular and
squamosal) coincide precisely with the dorso-lateral margins of the hyomandibular
and palatoquadrate, and thus with the distal margins of the diverticulum, so that the
ligament covers the diverticulum exactly.
In other crossopterygians (say, coelacanths
or dipnoans) this coincidence of dermal and
visceral bone-margins is not found; of course,
there also is no evidence of a diverticulum
in these forms. In Osteolepis, however, there
appears to have been a diverticulum present
(Thomson, personal communication), and
the external skull matches this by showing
a slit similar to that of Eusthenopteron
(Fig. 2, B). The conclusion is now inescapable that the diverticulum indeed ends
blindly, as I had previously only assumed.
5
1 used Jarvik's terminology here, although it
is somewhat different from standard nomenclature;
what Jarvik calls intertemporal and supratemporal,
for instance, are usually known as siipratenipoial
and tabular, respectively.
EVOLUTION OF HEARING IN VERTEBRATES
375
There appears to be no reason why we cannot take the situation one step further, and
propose that the diverticulum applied itself
intimately to the ligament, thus forming a
double-layered membrane. The inner layer
of this membrane is then the entoderm of
the diverticulum, while the outer layer is
an ectodermal ligament. This hypothetical
membrane is a precise homologue of the
tympanic membrane that is recognized in
tetrapods. It would appear, therefore, that
we may hypothesize that in the rhipidistians
SPIRACLE
FIG. 3. Schema to explain the effect of asymmetrical placement ol an air bubble in tissue. See
text.
FRONTAL
INTERTEMPORAL
PARIETAL
SUPRATEMPORAL
POSTSPIRACULAR
OPERCULAR
SQUAMOSAL
MAXILLARY
MANDIBLE
SUBORBITAL
10 MM
A
SPIRACLE
KIG. 2. A. Reconstructed skull of Eusthenopteron,
largely after Jarvik. (1954) and Goodrich (1930).
The black area behind the spiracle is the eardrum.
B. Skull of Osleolepis (after Goodrich, 1930). also
showing drum area in black. As noted in the text,
the black areas represent the maximal possible
extent of the drum; it is probably smaller.
the eardrum was already established as a
long, narrow, double-layered membrane between the squamosal and parietal shields;
this membrane constituted the distal surface
of a spiracular diverticulum which was
probably filled with air, and thus constituted a middle-ear cavity. The size of this
presumed drum membrane, as shown in
Figure 2, is what I would consider its
maximal possible extent; Thomson (personal communication) thinks it should be
much sinaller, perhaps only half as long.
As we shall see in a moment, there is a
functional advantage to this also.
At this point it is well to return briefly
to the question of how this drum membrane
can offset the disadvantage suffered by a
rhipidistian emerging into air where the
sound pressure is 36 dB less than it is in
water. Consider a spherical air bubble in
water with a surface area, A, as shown in
Figure 3, upper left. Subjecting this bubble
to a pressure change will change its volume
by AV. The resulting displacement of the
bubble's surface, d, is the quotient of
AV
volume and area: d =
. If we embed
A
this bubble inside a mantle of non-elastic
living tissue, and suspend the entire assembly in water (Fig. ?>, upper right), nothing
changes in the behavior of the bubble under
376
WlLLEM A. VAN BERGEIJK
pressure, because the density of the tissue
is very nearly that of water, and the resulting inertial load is symmetrically disposed.
Even when the bubble is moved to an asymmetrical position within the tissue (Fig. 3,
lower left), so that a thin membrane with
surface area, a, is created, nothing changes
in the bubble's behavior, because the inertial load is still symmetrical. But when the
asymmetrical assembly is put in air (Fig.
3, lower right), the situation changes drastically. The inertial load on the membrane
is now virtually nil, while on the rest of the
bubble the load of the tissue is still present.
The result is that in dynamic operation essentially the entire change of volume is
taken up by the membrane, producing a disAV
placement, d' =
, where d' is greater
a
than d by a factor A/a. This amplification
of d can be seen to increase as a becomes
smaller with respect to A. Of course, this
would only be true if the tissue mantle had
an effective mass that is infinite compared
to the mass of the membrane, or if the
mantle were completely rigid. In actuality,
those conditions may be met with varying
degrees of exactitude. What is important,
however, is that some degree of asymmetry
allows a fairly small part of the bubble's
surface to move with considerably greater
ease than the rest.
What, then, should the ratio, A/a, be if
the drop in pressure encountered in going
from water to air is to be compensated?
Clearly, if for the same change in pressure
(and so, the same AV) the asymmetrical
bubble shows a greater displacement of the
moveable surface in air, then less pressure is
necessary in air to produce the same displacement that would ensue in water for a
given pressure. The calculation is simple:
a difference in pressure of 36 dB is a factor
of about 63, as we have seen already, and
thus A/a should be about 63.
Let us now return to Eusthetwpleron and
see how well-adapted its system is to the
transition from water to air. We note immediately that we have indeed an asymmetrical bubble with only a small part of
FIG. 4. Same part of skull as in Fig. 1, but with
rectangles superimposed to calculate approximate
ratio of drum surface, C, to diverticulum surface,
2(A+B). See text.
its surface exposed, and the rest enclosed in
what clearly is a rather massive and perhaps
rigid jacket consisting of the hyomandibular
and parotic dental plates, and the palatoquadrate. The surface ratio, A/a, has, of
course, never been measured, but a ballpark approximation can be made on the
basis of Jarvik's figure. In Figure 4, this
drawing is shown again, but now with three
rectangles superimposed. Rectangles A and
B approximate my best guess about the
outline of the diverticulum; small rectangle
C represents the drum membrane. The total surface of A -|- B, multiplied by two to
take in the other side of the sac, and then
divided by the area of C, yields a quotient
of about 50. This corresponds to an increase of pressure-sensitivity of 34 dB. This
figure is gratifyingly close to the theoretical
value, and, in view of the very rough approximations we have had to make (especially the probably exaggerated size of
the drum) in the absence of precise measurements, may be taken to indicate that Eusthenopteron could have made the transition
from water to air with practically no loss
in acuity of hearing.
Having demonstrated that Eusthenopteron had an eardrum and was, at least on
physical grounds, quite capable of hearing
in air, we may next inquire how the drummembrane displacements were communi-
EVOLUTION OF HEARING IN VERTEBRATES
cated to the inner ear. The most obvious
(and, indeed, the only serious) candidate for
this function is the hyomandibular. It not
only forms the caudo-dorsal margin of the
endothelial side of the drum, but it also articulates directly with the otic capsule. The
homology of the hyomandibular and the
stapes of tetrapods is well-known and needs
no belaboring (see Goodrich, 1930, pp. 449485, for an extensive discussion). Until now,
however, the eardrum and stapes were assumed to have made their first appearance
in the primitive amphibians (Labyrinthodontia), since no recognizable precursor had
been demonstrated. The evidence presented
here pushes the origin of the eardrum-stapes
complex back to the ancestral fish, where it
appears to have been entirely functional for
hearing in air as well as underwater. Thus,
continuity in both structural and functional evolution is demonstrated.
ACKNOWLEDGMENT
For advice in matters physical I owe a debt to
G. G. Harris, whose patience with my ignorance
is immense.
377
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Harris, G. G. 1964. Considerations on the physics
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Harris, G. G., and W. A. van Bergeijk. 1962.
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