Evolution of mammalian auditory ossicles

Following on the ideas of Étienne Geoffroy Saint-Hilaire (1818), and studies by Johann Friedrich Meckel the Younger (1820), Carl Gustav Carus (1818), Martin Rathke (1825), and Karl Ernst von Baer (1828),[5] the relationship between the reptilian jaw bones and mammalian middle-ear bones was first established on the basis of embryology and comparative anatomy by Karl Bogislaus Reichert (in 1837, before the publication of On the Origin of Species in 1859). These ideas were advanced by Ernst Gaupp,[6] and are now known as the Reichert–Gaupp theory.[7][8]

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]

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 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 is not present in any of the early Triassic therapsids ("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 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]

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.

Mammalian and non-mammalian jaws. In the mammal configuration, the quadrate and articular bones are much smaller and form part of the middle ear. Note that in mammals the lower jaw consists of only the dentary bone.[24]

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]

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]

Morganucodontidae and other transitional forms had both types of jaw joint: dentary-squamosal (front) and articular-quadrate (rear).

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]

The earliest mammals were generally small animals, and were likely nocturnal insectivores. 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]

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][38]

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.[46] Hearing within mammals is further aided by a tympanum in the outer ear and newly evolved cochlea in the inner ear.

• Evolution of mammals
• Yanoconodon
• quadrate bone
• articular bone
• columella

• Your Inner Fish : We Hear With the Bones That Reptiles Eat With (video by Karen Sears and Neil Shubin