The evolution of mammalian auditory ossicles was an
evolutionary process that resulted in the formation of the bones of the mammalian
middle ear. These bones, or ossicles, are a defining characteristic of all
mammals. The event is well-documented[1] and important[2][3] as a demonstration of
transitional forms and
exaptation, the re-purposing of existing structures during evolution.[4]
The ossicles evolved from skull bones present in most
tetrapods, including the
reptilian lineage. The reptilian
quadrate bone,
articular bone, and
columella evolved into the mammalian
incus,
malleus, and
stapes (anvil, hammer, and stirrup), respectively.
In reptiles, the eardrum is connected to the inner ear via a single bone, the
columella, while the upper and lower jaws contain several bones not found in mammals. Over the course of the evolution of mammals, one bone from the lower and one from the upper jaw (the
articular and
quadrate bones) lost their function in the jaw joint and migrated to the middle ear. The shortened columella connected to these bones within the middle ear to form a chain of three bones, the
ossicles, which serve to effectively transmit air-based vibrations and facilitate more acute hearing.
The discovery of the link in
homology between the reptilian jaw joint and mammalian malleus and incus is considered an important milestone in the history of comparative anatomy.[9] Work on extinct
theromorphs by
Owen (1845), and continued by
Seeley,
Broom, and Watson, was pivotal in discovering the intermediate steps to this change.[10] The transition between the "reptilian" jaw and the "mammalian" middle ear was not bridged in the fossil record until the 1950s[11] with the elaboration of such fossils as the now-famous Morganucodon.[12]
During embryonic development, the incus and malleus arise from the same
first pharyngeal arch as the
mandible and
maxilla, and are served by mandibular and maxillary division of the
trigeminal nerve.[13] Recent genetic studies are able to relate the development of the ossicles from the embryonic arch[14] to hypothesized evolutionary history.[15]Bapx1, also known as Nkx3.2 (a member of the NK2 class of
homeobox genes),[16] is implicated in the change from the jaw bones of non-mammals to the ossicles of mammals.[17][18] Other implicated genes include the Dlx genes, Prx genes, and Wnt genes.[19]
Defining characteristic of mammals
Living mammal species can be identified by the presence in females of
mammary glands which produce milk. Other features are required when classifying
fossils, since mammary glands and other soft-tissue features are not visible in fossils.
Paleontologists therefore use the ossicles as distinguishing bony features shared by all living mammals (including
monotremes), but not present in any of the early
Triassictherapsids ("
mammal-like reptiles").
Early amniotes had a jaw joint composed of the
articular (a small bone at the back of the lower jaw) and the
quadrate (a small bone at the back of the upper jaw). All non-mammalian amniotes use this system including
lizards,
crocodilians,
dinosaurs (and their descendants the
birds) and
therapsids; so the only
ossicle in their
middle ears is the
stapes. The mammalian jaw joint is composed of different skull bones, including the
dentary (the lower jaw bone which carries the teeth) and the
squamosal (another small skull bone). In mammals, the quadrate and articular bones have evolved into the
incus and
malleus bones in the middle ear.[20][21]
The mammalian
middle ear contains three tiny bones known as the
ossicles:
malleus,
incus, and
stapes. The ossicles are a complex system of
levers whose functions include: reducing the
amplitude of the vibrations; increasing the mechanical
force of vibrations; and thus improving the efficient transmission of sound energy from the eardrum to the
inner ear structures. The ossicles act as the mechanical analog of an electrical
transformer, matching the
mechanical impedance of vibrations in air to vibrations in the liquid of the
cochlea. The net effect of this
impedance matching is to greatly increase the overall sensitivity and upper frequency limits of mammalian hearing, as compared to reptilian hearing. The details of these structures and their effects vary noticeably between different mammal species, even when the species are as closely related as humans and
chimpanzees.[22]
Phylogeny
The following simplified
cladogram displays relationships between
tetrapods:
The first fully terrestrial
vertebrates were
amniotes, which developed in eggs with internal membranes which allowed the developing
embryo to breathe but kept water in. The first amniotes arose in the late
Carboniferous from the ancestral
reptiliomorphs (a group of amphibians whose only living descendants are amniotes). Within a few million years two important amniote lineages became distinct: the
synapsid ancestors of mammals, and the
sauropsids ancestors of
lizards,
snakes,
crocodilians,
dinosaurs and
birds.[23]
The evolution of mammalian jaw joints and ears did not occur simultaneously with the evolution of other mammalian features. In other words, jaw joints and ears do not define any except the most recent groups of mammals.
Early tetrapod and amniote ears
In modern amniotes (including mammals), the middle ear collects airborne sounds through an
eardrum and transmits vibrations to the inner ear via thin cartilaginous and ossified structures. These structures usually include the
stapes (a
stirrup-shaped auditory ossicle).
Early
tetrapods likely did not possess eardrums. Eardrums appear to have evolved independently three to six times.[25][26] In basal members of the 3 major
clades of amniotes (synapsids,
eureptiles, and
parareptiles) the
stapes bones are relatively massive props that support the
braincase, and this function prevents them from being used as part of the hearing system. However, there is increasing evidence that synapsids, eureptiles and parareptiles developed eardrums connected to the inner ear by stapes during the
Permian.[27]
Early therapsid jaws and ears
The jaws of early synapsids, including the ancestors of mammals, were similar to those of other
tetrapods of the time, with a lower jaw consisting of a
tooth-bearing dentary bone and several smaller posterior bones. The jaw joint consisted of the
articular bone in the lower jaw and the
quadrate in the upper jaw. The early
pelycosaurs (late Carboniferous and
early Permian) likely did not have
tympanic membranes (external eardrums). Additionally, their massive stapes bones supported the braincase, with the lower ends resting on the quadrates. Their descendants, the
therapsids (including mammalian ancestors), probably had tympanic membranes in contact with the quadrate bones. The stapes remained in contact with the quadrate bone, but functioned as auditory ossicles rather than supports for the brain case. As a result, the quadrate bones of therapsids likely had a dual function in both the jaw joint and auditory system.[28][29]
Twin-jointed jaws
During the
Permian and early
Triassic the dentary of therapsids, including the ancestors of mammals, continually enlarged while other jaw bones were reduced.[30]
Eventually, the dentary bone evolved to make contact with the
squamosal, a bone in the upper jaw located
anterior to the quadrate, allowing two simultaneous jaw joints:[31] an anterior "
mammalian" joint between the dentary and squamosal and a
posterior "reptilian" joint between the quadrate and articular. This "twin-jointed jaw" can be seen in late
cynodonts and early
mammaliforms.[32]Morganucodon is one of the first discovered and most thoroughly studied of the mammaliforms, since an unusually large number of morganucodont fossils have been found. It is an example of a nearly perfect evolutionary intermediate between the mammal-like reptiles and extant reptiles.[33]
Early mammals
The earliest mammals were generally small animals, and were likely
nocturnalinsectivores. This suggests a plausible source of evolutionary pressure: with these small bones in the middle ear, a mammal has extended its range of hearing for higher-pitched sounds which would improve the detection of insects in the dark.[34]
The evidence that the malleus and incus are
homologous to the reptilian articular and quadrate was originally embryological, and since this discovery an abundance of
transitional fossils has both supported the conclusion and given a detailed history of the transition.[35] The evolution of the
stapes (from the
columella) was an earlier and distinct event.[36][37]
The evolution of the mammalian middle ear appears to have occurred in two steps. A partial middle ear formed by the departure of postdentary bones from the dentary, and happened independently in the ancestors of monotremes and
therians. The second step was the transition to a definite mammalian middle ear, and evolved independently at least three times in the ancestors of todays monotremes, marsupials and placentalians.[38]
Fossil evidence for mammal-like jaws and ears
As the dentary bone of the lower jaw continued to enlarge during the Triassic, the older quadrate-articular joint fell out of use. Some of the bones were lost, but the
quadrate, the
articular, and the
angular bones became free-floating and associated with the
stapes. This occurred at least twice in the
mammaliformes. The
multituberculates had jaw joints that consisted of only the dentary and squamosal bones, and the quadrate and articular bones were part of the middle ear. Other features of their teeth, jaws and skulls are significantly different from those of mammals.[21][39]
Hadrocodium
In the lineage most closely related to mammals, the jaws of Hadrocodium (about 195M years ago in the very early Jurassic) suggest that it may have been the first to have a nearly fully mammalian middle ear: it lacks the trough at the rear of the lower jaw, over which the eardrum stretched in therapsids and earlier mammaliformes. The absence of this trough suggests that Hadrocodium’s ear was part of the cranium, as it is in mammals, and that the former articular and quadrate had migrated to the middle ear and become the malleus and incus. Hadrocodium’s dentary has a "bay" at the rear which mammals lack, a hint that the dentary bone retained the same shape as if the articular and quadrate had remained part of the jaw joint.[40] However, several studies have cast doubt on whether Hadrocodium did indeed possess a definitive mammalian middle ear; Hadrocodium likely had an ossified connection between the middle ear and the jaw, which is not visible in the fossil evidence due to limited preservation.[41][42] Researchers now hypothesize that the definitive mammalian middle ear did not emerge any earlier than the late Jurassic (~163M years ago).[42]
Teinolophos
It has been suggested that a relatively large trough in the jaw bone of the early Cretaceous
monotremeTeinolophos provides evidence of a pre-mammalian jaw joint, because therapsids and many mammaliforms had such troughs in which the articular and angular bones "docked". Thus, Teinolophos had a pre-mammalian middle ear, indicating that the mammalian middle ear ossicles evolved independently in monotremes and in other mammals.[43] A more recent analysis of Teinolophos concluded that the trough was a channel for the large vibration and electrical sensory nerves terminating in the bill (a defining feature of the modern platypus). Thus, the trough is not evidence that Teinolophos had a pre-mammalian jaw joint and a pre-mammalian middle ear.[44]
Yanoconodon
A recently discovered intermediate form is the primitive mammal Yanoconodon, which lived approximately 125 million years ago in the
Mesozoic era. In Yanoconodon the ossicles have separated from the jaw and serve the hearing function in the middle ear, yet maintain a slender connection to the jaw via the ossified
Meckel's cartilage.[45][42] Maintaining a connection via the ossified Meckel's cartilage may have been evolutionary advantageous since the auditory ossicles were not connected to the cranium in Yanoconodon (as they are in
extant mammals), and required structural support via Meckel's cartilage.[46]
Effects on hearing
The
frequency range and sensitivity of the
ear is dependent on the shape and arrangement of the middle-ear bones. In the reptilian lineage, hearing depends on the conduction of low-frequency vibrations through the ground or bony structures (such as the
columella). By modifying the articular bone, quadrate bone, and columella into small ossicles, mammals were able to hear a wider range of high-frequency airborne vibrations.[47] Hearing within mammals is further aided by a
tympanum in the outer ear and newly evolved
cochlea in the inner ear.
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