Theevolution of mammalian auditory ossicles was anevolutionary process that resulted in the formation of themammalianmiddle ear, where the three middle ear bones orossicles, namely theincus,malleus andstapes (a.k.a. "the anvil, hammer, and stirrup"), are a defining characteristic of mammals. The event is well-documented[1] and important[2][3] academically as a demonstration oftransitional forms andexaptation, the re-purposing of existing structures during evolution.[4]
The ossicles evolved from skull bones present in mosttetrapods, includingamphibians,sauropsids (which includeextantreptiles andbirds) and earlysynapsids (which include ancestors of mammals). The reptilianquadrate,articular andcolumella bones arehomologs of the mammalian incus, malleus and stapes, respectively. In reptiles (and early synapsids by association), theeardrum is connected to theinner ear via a single bone, the columella, while the upper and lower jaws contain several bones not found in modern mammals. Over the course ofmammalian evolution, one bone from the upper jaw (the quadrate) and one from the lower jaw (the articular) lost their function in the jaw articulation and migrated to form the middle ear. The shortened columella connected to these bones to form akinematic chain of three ossicles, which serve toamplify air-sourced fine vibrations transmitted from the eardrum and facilitate more acutehearing in terrestrial environments.
The discovery of the link inhomology between the reptilian jaw joint and mammalian malleus and incus is considered an important milestone in the history of comparative anatomy.[11] Work on extincttheromorphs byOwen (1845), and continued bySeeley,Broom, and Watson, was pivotal in discovering the intermediate steps to this change.[12] The transition between the "reptilian" jaw and the "mammalian" middle ear was not bridged in thefossil record until the 1950s[13] with the elaboration of such fossils as the now-famousMorganucodon.[14]
During embryonic development, the incus and malleus arise from the samefirst pharyngeal arch as themandible andmaxilla, and are served by mandibular and maxillary division of thetrigeminal nerve.[15] Recent genetic studies are able to relate the development of the ossicles from the embryonic arch[16] to hypothesized evolutionary history.[17]Bapx1, also known asNkx3.2 (a member of the NK2 class ofhomeobox genes),[18] is implicated in the change from the jaw bones of non-mammals to the ossicles of mammals.[19][20] Other implicated genes include theDlx genes,Prx genes, andWnt genes.[21]
A typical mammalian middle ear: sound makes the tympanum (eardrum) vibrate; 3 small bones, the malleus, incus and stapes, transmit the vibrations to the labyrinth (inner ear), which transforms the vibrations into nerve signals.
Living mammal species can be identified by the presence in females ofmammary glands which produce milk. Other features are required when classifyingfossils, 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 (includingmonotremes), but not present in any of the earlyTriassictherapsids ("mammal-like reptiles").
Upper and lower portions of a python skull, displaying multiple bony components of the upper and lower jaws. Courtesy of the Peabody Museum of Natural History; Division of Vertebrate Zoology; Yale University.
Early amniotes had a jaw joint composed of thearticular (a small bone at the back of the lower jaw) and thequadrate (a small bone at the back of the upper jaw). All non-mammalian amniotes use this system includinglizards,crocodilians,dinosaurs (and their descendants thebirds) andtherapsids; so the onlyossicle in theirmiddle ears is thestapes. The mammalian jaw joint is composed of different skull bones, including thedentary (the lower jaw bone which carries the teeth) and thesquamosal (another small skull bone). In mammals, the quadrate and articular bones have evolved into theincus andmalleus bones in the middle ear.[22][23]
The mammalianmiddle ear contains three tiny bones known as theossicles:malleus,incus, andstapes. The ossicles are a complex system oflevers whose functions include: reducing theamplitude of the vibrations; increasing the mechanicalforce of vibrations; and thus improving the efficient transmission of sound energy from the eardrum to theinner ear structures. The ossicles act as the mechanical analog of an electricaltransformer, matching themechanical impedance of vibrations in air to vibrations in the liquid of thecochlea. The net effect of thisimpedance 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 andchimpanzees.[24]
The first fully terrestrialvertebrates wereamniotes, which developed in eggs with internal membranes which allowed the developingembryo to breathe but kept water in. The first amniotes arose in the lateCarboniferous from the ancestralreptiliomorphs (a group of amphibians whose only living descendants are amniotes). Within a few million years two important amniote lineages became distinct: thesynapsid ancestors of mammals, and thesauropsids ancestors oflizards,snakes,crocodilians,dinosaurs andbirds.[25]
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.
Mammalian and non-mammalian jaws. In the mammal configuration, thequadrate andarticular bones are much smaller and form part of the middle ear. Note that in mammals the lower jaw consists of only thedentary bone.[26]
In modern amniotes (including mammals), the middle ear collects airborne sounds through aneardrum and transmits vibrations to the inner ear via thin cartilaginous and ossified structures. These structures usually include thestapes (astirrup-shaped auditory ossicle).
Earlytetrapods likely did not possess eardrums. Eardrums appear to have evolved independently three to six times.[27][28] In basal members of the 3 majorclades of amniotes (synapsids,eureptiles, andparareptiles) thestapes bones are relatively massive props that support thebraincase, 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 thePermian.[29]
The jaws of early synapsids, including the ancestors of mammals, were similar to those of othertetrapods of the time, with a lower jaw consisting of atooth-bearing dentary bone and several smaller posterior bones. The jaw joint consisted of thearticular bone in the lower jaw and thequadrate in the upper jaw. The earlypelycosaurs (late Carboniferous andearly Permian) likely did not havetympanic membranes (external eardrums). Additionally, their massive stapes bones supported the braincase, with the lower ends resting on the quadrates. Their descendants, thetherapsids (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.[30][31]
During thePermian and earlyTriassic the dentary of therapsids, including the ancestors of mammals, continually enlarged while other jaw bones were reduced.[32]
Eventually, the dentary bone evolved to make contact with thesquamosal, a bone in the upper jaw locatedanterior to the quadrate, allowing two simultaneous jaw joints:[33] an anterior "mammalian" joint between the dentary and squamosal and aposterior "reptilian" joint between the quadrate and articular. This "twin-jointed jaw" can be seen in latecynodonts and earlymammaliforms.[34]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 mammals.[35]
The earliest mammals were generally small animals, and were likelynocturnalinsectivores. 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.[36]
The evidence that the malleus and incus arehomologous to the reptilian articular and quadrate was originally embryological, and since this discovery an abundance oftransitional fossils has both supported the conclusion and given a detailed history of the transition.[37] The evolution of thestapes (from thecolumella) was an earlier and distinct event.[38][39]
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 andtherians. The second step was the transition to a definite mammalian middle ear, and evolved independently at least three times in the ancestors of today's monotremes, marsupials and placentals.[40]
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 thequadrate, thearticular, and theangular bones became free-floating and associated with thestapes. This occurred at least twice in themammaliformes. Themultituberculates 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.[23][41]
In the lineage most closely related to mammals, the jaws ofHadrocodium (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 thatHadrocodium'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.[42] However, several studies have cast doubt on whetherHadrocodium 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.[43][44] Researchers now hypothesize that the definitive mammalian middle ear did not emerge any earlier than the late Jurassic (~163M years ago).[44]
It has been suggested that a relatively large trough in the jaw bone of the early CretaceousmonotremeTeinolophos 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.[45] A more recent analysis ofTeinolophos 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 thatTeinolophos had a pre-mammalian jaw joint and a pre-mammalian middle ear.[46]
A recently discovered intermediate form is the primitive mammalYanoconodon, which lived approximately 125 million years ago in theMesozoic era. InYanoconodon 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 ossifiedMeckel's cartilage.[47][44] Maintaining a connection via the ossified Meckel's cartilage may have been evolutionary advantageous since the auditory ossicles were not connected to the cranium inYanoconodon (as they are inextant mammals), and required structural support via Meckel's cartilage.[48]
Thefrequency range and sensitivity of theear 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 thecolumella). 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.[49] Hearing within mammals is further aided by atympanum in the outer ear and an elongated lagena (cochlea) in the inner ear.
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