Evolution of mammalian auditory ossicles
Encyclopedia
The evolution of mammalian auditory ossicles is one of the most well-documented and important evolution
ary events, demonstrating both numerous transitional forms
as well as an excellent example of exaptation
, the re-purposing of existing structures during evolution.
In reptiles, the eardrum is connected to the inner ear via a single bone, the stapes or stirrup, while the upper and lower jaws contain several bones not found in mammals. Over the course of the evolution of mammals, one lower and one upper jaw bone (the articular
and quadrate) lost their purpose in the jaw joint and were put to new use in the middle ear, connecting to the stapes and forming a chain of three bones (collectively called the ossicles
) which amplify sounds and allow more acute hearing. In mammals, these three bones are known as the malleus
, incus
, and stapes (hammer, anvil, and stirrup respectively).
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 fossil
s has both supported the conclusion and given a detailed history of the transition. The evolution of the stapes was an earlier and distinct event.
and comparative anatomy
by Reichert
(in 1837, before the publication of On the Origin of Species in 1859) and advanced by Gaupp
, and this is known as the Reichert–Gaupp Theory.
In the course of the development of the embryo, 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 Cranial nerve.
There are also more recent studies in the genetic basis for the development of the ossicles from the embryonic arch. and relating this to evolutionary history.
"Bapx1, also known as Nkx3.2
, is the vertebrate homologue of the Drosophila gene Bagpipe. A member of the NK2 class of homeobox
genes ..." and this gene is implicated in the change from the jaw bones of non-mammals to the ossicles of mammals. Yet the transition between the "reptilian" jaw and the "mammalian" inner ear was not bridged in the fossil record until the 1950s with the elaboration of such fossils as the now-famous Morganucodon
.
Image:Mammal middle ear.png | thumb | right | 251px | A typical mammalian middle ear: sound makes the tympanum (ear-drum) vibrate; 3 small bones, the malleus, incus and stapes, transmit the vibrations to the Labyrinth (inner ear), which transforms the vibrations into nerve signals.
rect 30 14 118 28 Tensor tympani
rect 146 48 181 60 Incus
rect 169 65 227 77 Stapedius
rect 177 100 231 113 Labyrinth
rect 164 116 205 130 Stapes
rect 154 136 242 151 Tympanic cavity
rect 165 165 226 194 Eustachian Tube
rect 18 164 132 194 Ear drum
rect 5 138 87 151 Ear canal
rect 28 56 74 71 Malleus
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 amount of energy transmitted. The details of these effects vary noticeably between different mammal species, even when the species are as closely related as humans and chimpanzees.
s 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 a distinguishing feature that is shared by all living mammals (including monotremes), but is not present in any of the early Triassic
therapsids ("mammal-like reptiles"): mammals use two bones for hearing that all other amniotes use for eating. The earliest 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, dinosaur
s (and their descendants the birds) and therapsids; so the only ossicle in their middle ear
s is the stapes. But mammals have a different jaw joint, composed only of the dentary (the lower jaw bone which carries the teeth) and the squamosal
(another small skull bone). And in mammals the quadrate and articular bones have become the incus
and malleus
bones in the middle ear.
--Tetrapod
s------
| ("4 legged"; the earliest breathed via gills)
|
+-- Amphibian
s ----------------------------------------------
|
`--------Reptiliomorph
s-----
| ("reptile-like" amphibians)
|
`--Amniote
s------
|
+--Sauropsids ("lizard faces")---------------
| (lizards, crocodilians, dinosaur
s, birds
| Testudines; and some extinct groups)
|
`--Synapsid
s------
|
`--Pelycosaur
s----
|
`--Therapsids-----
|
`--Mammal
s---------------
The first fully terrestrial vertebrate
s were amniotes - their eggs had internal membranes which allowed the developing embryo
to breathe but kept water in. This allowed amniotes to lay eggs on dry land, while amphibians generally need to lay their eggs in water. The first amniotes apparently arose in the late Carboniferous
from the ancestral reptiliomorph
s (a group of amphibians whose only living descendants are amniotes). Within a few million years two important amniote lineages became distinct: mammals' synapsid
ancestors and the sauropsids, from which lizard
s, snake
s, crocodilians, dinosaur
s and bird
s are descended.
The earliest known fossils of all these groups date from about 320 to 315M years ago. Unfortunately it is difficult to be sure about when each of them evolved, since vertebrate fossils from the late Carboniferous are very rare, and therefore the actual first occurrences of each of these types of animal might have been considerably earlier.
The pattern in most of the following sections is that each successive more "advanced" group started with the more "primitive" jaws and ears of its predecessors, then developed more mammal-like jaws and ears, and so on. The evolution of mammalian jaw joints and ears did not proceed neatly in step with the evolution of other mammalian features; or, to put it another way, all but the last of the various stages into which paleontologists divide the evolution towards the mammalian condition are not defined by their jaw joints and ears.
-shaped auditory ossicle). But the earliest tetrapods, amphibians and amniotes probably did not have ear drums. In fact ear drums apparently evolved independently three to six times, in: stegocephalians (very primitive amphibians); in anurans (the amphibian group that includes frogs and toads); in synapsids (mammals and their extinct relatives), in diapsids (the most important sauropsid group, including lizards, crocodiles, dinosaurs and birds); perhaps separately in anapsids (turtles and their extinct relatives), if turtles are not modified diapsids; probably in seymouriamorphs
(a group of reptiliomorphs); and possibly in some temnospondyls
(primitive amphibians). In all 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. But there is increasing evidence that synapsids, eureptiles and parareptiles developed eardrums connected to the inner ear by stapes during the Permian
.
s 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) most probably did not have tympanic membranes (external eardrums), and their massive stapes bones supported the braincase, with the lower ends resting on the quadrates. But their descendants the therapsids (including mammals' ancestors) probably did have tympanic membranes and these probably were in contact with the quadrate bones; and the stapes bones were still in contact with the quadrates but functioned as auditory ossicles rather than braincase supports; so the therapsids' quadrates had a dual function, as part of the jaw joint and as parts of the hearing system.
During the Permian
and early Triassic
the dentary of therapsids, including the ancestors of mammals, continually enlarged while other jaw bones were reduced. Eventually, the dentary was able to make contact with the squamosal
, a bone in the upper jaw located anterior to the quadrate, allowing two simultaneous jaw joints - an anterior "mammal
ian" 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 cynodont
s and early mammaliforms
. 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, and
) to about 35M years ago (early Oligocene) had jaw joints that consisted of only the dentary and squamosal bones, and the quadrate and articular bones were part of the middle ear; but other features of their teeth, jaws and skulls are significantly different from those of mammals.
In the lineage most closely related to mammals, the jaws of Hadrocodium
(about 195M years ago in the very early Jurassic) suggest that it or a very close ancestor 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, and the absence of this trough which suggests that Hadrocodium’s ear was part of the cranium, as it is in mammals, and hence that the former articular and quadrate had migrated to the middle ear and become the malleus and incus; but Hadrocodium’s dentary has a "bay" at the rear which mammals lack, a hint that that its dentary bone retained the same shape that it would have had if the articular and quadrate had remained part of the jaw joint. It has been suggested that a relatively large trough in the jaw bone of the early Cretaceous monotreme
Teinolophos
provides evidence of a pre-mammalian jaw joint, because therapsids and many mammaliforms had such troughs, in which the articular and angular bones "docked", and therefore that Teinolophos had a pre-mammalian middle ear; and therefore that the mammalian middle ear ossicles evolved indepedendently in monotremes and in other mammals. But a more recent analysis of Teinolophos concluded that the animal was a full-fledged platypus
and the trough was a channel for the large number of nerves that collect signals from the electrical and vibration sensors in the bill (this is a signature feature of the platypi within monotremes), and therefore that the trough is not evidence that Teinolophos had a pre-mammalian jaw joint and a pre-mammalian middle ear. Ironically Rich and Vickers-Rich were among the authors of the 2005 paper on which they later cast doubt.
A recently discovered intermediate form is the primitive mammal Yanoconodon
, from 125 million years ago in the Mesozoic
, in which 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
, which in more advanced mammals dissolves during development.
and sensitivity of the ear
is dependent upon the shape and arrangement of the middle-ear bones. In early synapsids such as the pelycosaurs, the quadrate and articular had to function as the jaw joint, and this severely limited how far these bones could be modified to alter the frequency range of the ear. But once these bones were no longer involved in the jaw joint, variations which affected hearing would not also affect jaw joint function, and this allowed unconstrained evolution of the mammalian hearing apparatus. By the Jurassic
, the typical mammalian ear had evolved, in which the angular had become the tympanic annula (a bony support for the tympanic membrane), while the articular and quadrate had become the malleus
and incus
, respectively, connected in series with the stapes. This series of three bones acts as an amplification
system to allow enhanced hearing.
The transition between these two states is one of the most well-documented and supported in all of evolution, and newly discovered fossils from this transitional period have recently improved our understanding of this transition. But they also suggest that it was not a simple linear process from the early therapsid jaw (quadrate-articular joint) and middle ear (with stapes as the only ossicles) to the modern mammalian condition.
could be a factor in the preservation of the structure of the middle ear in mammals. Many of the earliest mammals were quite small, and the dentition indicates that they were insectivorous. If they were "warm-blooded
" (endothermic), like modern mammals, then they could have been nocturnal. This fits with the popular image of small, nocturnal insectivorous mammals surviving in niches not accessible to the large, dominant contemporary dinosaurs. The enhanced hearing, particularly in the higher frequencies, would be helpful for nocturnal animals, in particular for detecting insects. This scenario is consistent with selective advantage being a contributory factor to the transition.
As evolutionary biology began to be expanded upon, this relationship became treated as one of common descent. For the evolutionary explanation to make sense, it seemed to demand that there would be a transition in function between being part of the feeding mechanism in the joint of the jaw and serving only in hearing; and this would mean that somehow there had to be an intermediate connecting these two quite different functions. With the discovery of Morganucodon and other fossils, there were concrete examples of this. There was a double jaw joint: the "older reptilian", as well as the "newer mammalian", in the same animal. This meant a confirmation of the pattern of inference from comparative anatomy to evolutionary biology.
The earliest mammals were generally small animals, probably nocturnal insectivores. This suggests a plausible evolutionary mechanism driving the change, for 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. Natural selection would account for the success of this feature. And still one more connection with another part of biology: genetics suggested a mechanism for this transition, the kind of major change of function seen elsewhere in the world of life being studied by Evodevo.
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
ary events, demonstrating both numerous transitional forms
Transitional fossil
A transitional fossil is any fossilized remains of a lifeform that exhibits characteristics of two distinct taxonomic groups. A transitional fossil is the fossil of an organism near the branching point where major individual lineages diverge...
as well as an excellent example of exaptation
Exaptation
Exaptation, cooption, and preadaptation are related terms referring to shifts in the function of a trait during evolution. For example, a trait can evolve because it served one particular function, but subsequently it may come to serve another. Exaptations are common in both anatomy and behaviour...
, the re-purposing of existing structures during evolution.
In reptiles, the eardrum is connected to the inner ear via a single bone, the stapes or stirrup, while the upper and lower jaws contain several bones not found in mammals. Over the course of the evolution of mammals, one lower and one upper jaw bone (the articular
Articular
The articular bone is part of the lower jaw of most tetrapods, including amphibians, sauropsids and early synapsids. In these animals it is connected to two other lower jaw bones, the suprangular and the angular...
and quadrate) lost their purpose in the jaw joint and were put to new use in the middle ear, connecting to the stapes and forming a chain of three bones (collectively called the ossicles
Ossicles
The ossicles are the three smallest bones in the human body. They are contained within the middle ear space and serve to transmit sounds from the air to the fluid-filled labyrinth . The absence of the auditory ossicles would constitute a moderate-to-severe hearing loss...
) which amplify sounds and allow more acute hearing. In mammals, these three bones are known as the malleus
Malleus
The malleus or hammer is a hammer-shaped small bone or ossicle of the middle ear which connects with the incus and is attached to the inner surface of the eardrum...
, incus
Incus
The incus or anvil is the anvil-shaped small bone or ossicle in themiddle ear. It connects the malleus to the stapes. It was first described by Alessandro Achillini of Bologna.The incus transmits sound vibrations from the malleus to the stapes....
, and stapes (hammer, anvil, and stirrup respectively).
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 fossil
Transitional fossil
A transitional fossil is any fossilized remains of a lifeform that exhibits characteristics of two distinct taxonomic groups. A transitional fossil is the fossil of an organism near the branching point where major individual lineages diverge...
s has both supported the conclusion and given a detailed history of the transition. The evolution of the stapes was an earlier and distinct event.
Reichert–Gaupp theory
The relationship between the reptilian jaw bones and mammalian middle-ear bones was first established on the basis of embryologyEmbryology
Embryology is a science which is about the development of an embryo from the fertilization of the ovum to the fetus stage...
and comparative anatomy
Comparative anatomy
Comparative anatomy is the study of similarities and differences in the anatomy of organisms. It is closely related to evolutionary biology and phylogeny .-Description:...
by Reichert
Karl Bogislaus Reichert
Karl Bogislaus Reichert was a German anatomist.Reichert was born in Rastenburg , East Prussia. He studied etiology and histology in Königsberg. He was a student of Friedrich Schlemm and Johannes Peter Müller at the Friedrich-Wilhelm-Institute and at the Charité in Berlin, receiving his doctorate...
(in 1837, before the publication of On the Origin of Species in 1859) and advanced by Gaupp
Ernst Gaupp
Ernst Wilhelm Theodor Gaupp was a German anatomist from Beuthen in Upper Silesia . He studied natural sciences and medicine in Jena, Königsberg and Breslau, where he received his doctorate in 1889...
, and this is known as the Reichert–Gaupp Theory.
In the course of the development of the embryo, the incus and malleus arise from the same First Pharyngeal arch as the Mandible
Mandible
The mandible pronunciation or inferior maxillary bone forms the lower jaw and holds the lower teeth in place...
and Maxilla
Maxilla
The maxilla is a fusion of two bones along the palatal fissure that form the upper jaw. This is similar to the mandible , which is also a fusion of two halves at the mental symphysis. Sometimes The maxilla (plural: maxillae) is a fusion of two bones along the palatal fissure that form the upper...
, and are served by mandibular and maxillary division of the Trigeminal Cranial nerve.
...the discovery that the mammalian malleus and incus were actually homologues of visceral elements of the "reptilian" jaw articulation ... ranks as one of the milestones in the history of comparative biology.
... it is one of the triumphs of the long series of researches on the extinct Theromorph reptiles, begun by OwenRichard OwenSir Richard Owen, FRS KCB was an English biologist, comparative anatomist and palaeontologist.Owen is probably best remembered today for coining the word Dinosauria and for his outspoken opposition to Charles Darwin's theory of evolution by natural selection...
(1845), and continued by SeeleyHarry SeeleyHarry Govier Seeley was a British paleontologist.-Career:Seeley was born in London, the son of Richard Hovill Seeley, goldsmith, and his second wife Mary Govier. He attended classes at the Royal School of Mines, Kensington before becoming an assistant to Adam Sedgwick at the Woodwardian Museum,...
, BroomRobert BroomProfessor Robert Broom was a Scottish South African doctor and paleontologist. He qualified as a medical practitioner in 1895 and received his DSc in 1905 from the University of Glasgow...
, and Watson, to have revealed the intermediate steps by which the change may have occurred from an inner quadrate to an outer squamosal articulation ...
There are also more recent studies in the genetic basis for the development of the ossicles from the embryonic arch. and relating this to evolutionary history.
"Bapx1, also known as Nkx3.2
NKX3-2
NK3 homeobox 2 also known as NKX3-2 is a human gene. It is a homolog of bagpipe in Drosophila and therefore also known as Bapx1 . The protein encoded by this gene is a homeo domain containing transcription factor.-Function:NKX3-2 plays a role in the development of the skeleton...
, is the vertebrate homologue of the Drosophila gene Bagpipe. A member of the NK2 class of homeobox
Homeobox
A homeobox is a DNA sequence found within genes that are involved in the regulation of patterns of anatomical development in animals, fungi and plants.- Discovery :...
genes ..." and this gene is implicated in the change from the jaw bones of non-mammals to the ossicles of mammals. Yet the transition between the "reptilian" jaw and the "mammalian" inner ear was not bridged in the fossil record until the 1950s with the elaboration of such fossils as the now-famous Morganucodon
Morganucodon
Morganucodon is an early mammalian genus which lived during the Late Triassic. It first appeared about 205 million years ago. This has also been identified with Eozostrodon. Unlike many other early mammals, Morganucodon is well represented by abundant and well preserved, though in the vast...
.
Image:Mammal middle ear.png | thumb | right | 251px | A typical mammalian middle ear: sound makes the tympanum (ear-drum) vibrate; 3 small bones, the malleus, incus and stapes, transmit the vibrations to the Labyrinth (inner ear), which transforms the vibrations into nerve signals.
rect 30 14 118 28 Tensor tympani
Tensor tympani
The tensor tympani, the larger of the two muscles of the tympanic cavity, is contained in the bony canal above the osseous portion of the auditory tube...
rect 146 48 181 60 Incus
Incus
The incus or anvil is the anvil-shaped small bone or ossicle in themiddle ear. It connects the malleus to the stapes. It was first described by Alessandro Achillini of Bologna.The incus transmits sound vibrations from the malleus to the stapes....
rect 169 65 227 77 Stapedius
Stapedius
The stapedius is the smallest skeletal muscle in the human body. At just over one millimeter in length, its purpose is to stabilize the smallest bone in the body, the stapes....
rect 177 100 231 113 Labyrinth
rect 164 116 205 130 Stapes
rect 154 136 242 151 Tympanic cavity
Tympanic cavity
The tympanic cavity is a small cavity surrounding the bones of the middle ear.It is formed from the tubotympanic recess, an expansion of the first pharyngeal pouch....
rect 165 165 226 194 Eustachian Tube
Eustachian tube
The Eustachian tube is a tube that links the nasopharynx to the middle ear. It is a part of the middle ear. In adult humans the Eustachian tube is approximately 35 mm long. It is named after the sixteenth-century anatomist Bartolomeo Eustachi...
rect 18 164 132 194 Ear drum
rect 5 138 87 151 Ear canal
Ear canal
The ear canal , is a tube running from the outer ear to the middle ear. The human ear canal extends from the pinna to the eardrum and is about 35 mm in length and 5 to 10 mm in diameter....
rect 28 56 74 71 Malleus
Malleus
The malleus or hammer is a hammer-shaped small bone or ossicle of the middle ear which connects with the incus and is attached to the inner surface of the eardrum...
- desc top-right
Definitive mammalian middle ear
The mammalian middle earMiddle ear
The middle ear is the portion of the ear internal to the eardrum, and external to the oval window of the cochlea. The mammalian middle ear contains three ossicles, which couple vibration of the eardrum into waves in the fluid and membranes of the inner ear. The hollow space of the middle ear has...
contains three tiny bones known as the ossicles
Ossicles
The ossicles are the three smallest bones in the human body. They are contained within the middle ear space and serve to transmit sounds from the air to the fluid-filled labyrinth . The absence of the auditory ossicles would constitute a moderate-to-severe hearing loss...
: malleus
Malleus
The malleus or hammer is a hammer-shaped small bone or ossicle of the middle ear which connects with the incus and is attached to the inner surface of the eardrum...
, incus
Incus
The incus or anvil is the anvil-shaped small bone or ossicle in themiddle ear. It connects the malleus to the stapes. It was first described by Alessandro Achillini of Bologna.The incus transmits sound vibrations from the malleus to the stapes....
, and stapes. The ossicles are a complex system of levers whose functions include: reducing the amplitude
Amplitude
Amplitude is the magnitude of change in the oscillating variable with each oscillation within an oscillating system. For example, sound waves in air are oscillations in atmospheric pressure and their amplitudes are proportional to the change in pressure during one oscillation...
of the vibrations; increasing the amount of energy transmitted. The details of these effects vary noticeably between different mammal species, even when the species are as closely related as humans and chimpanzees.
Definition of "mammal"
Living mammal species can be identified by the presence in females of mammary glandMammary gland
A mammary gland is an organ in mammals that produces milk to feed young offspring. Mammals get their name from the word "mammary". In ruminants such as cows, goats, and deer, the mammary glands are contained in their udders...
s which produce milk. Other features are required when classifying fossils, since mammary glands and other soft-tissue features are not visible in fossils. Paleontologists
Paleontology
Paleontology "old, ancient", ὄν, ὀντ- "being, creature", and λόγος "speech, thought") is the study of prehistoric life. It includes the study of fossils to determine organisms' evolution and interactions with each other and their environments...
therefore use a distinguishing feature that is shared by all living mammals (including monotremes), but is not present in any of the early Triassic
Triassic
The Triassic is a geologic period and system that extends from about 250 to 200 Mya . As the first period of the Mesozoic Era, the Triassic follows the Permian and is followed by the Jurassic. Both the start and end of the Triassic are marked by major extinction events...
therapsids ("mammal-like reptiles"): mammals use two bones for hearing that all other amniotes use for eating. The earliest amniotes had a jaw joint composed of the articular
Articular
The articular bone is part of the lower jaw of most tetrapods, including amphibians, sauropsids and early synapsids. In these animals it is connected to two other lower jaw bones, the suprangular and the angular...
(a small bone at the back of the lower jaw) and the quadrate
Quadrate bone
The quadrate bone is part of a skull in most tetrapods, including amphibians, sauropsids , and early synapsids. In these animals it connects to the quadratojugal and squamosal in the skull, and forms part of the jaw joint .- Evolutionary variation :In snakes, the quadrate bone has become elongated...
(a small bone at the back of the upper jaw). All non-mammalian amniotes use this system including lizards, crocodilians, dinosaur
Dinosaur
Dinosaurs are a diverse group of animals of the clade and superorder Dinosauria. They were the dominant terrestrial vertebrates for over 160 million years, from the late Triassic period until the end of the Cretaceous , when the Cretaceous–Paleogene extinction event led to the extinction of...
s (and their descendants the birds) and therapsids; so the only ossicle in their middle ear
Middle ear
The middle ear is the portion of the ear internal to the eardrum, and external to the oval window of the cochlea. The mammalian middle ear contains three ossicles, which couple vibration of the eardrum into waves in the fluid and membranes of the inner ear. The hollow space of the middle ear has...
s is the stapes. But mammals have a different jaw joint, composed only of the dentary (the lower jaw bone which carries the teeth) and the squamosal
Squamosal
The squamosal is a bone of the head of higher vertebrates. It is the principal component of the cheek region in the skull, lying below the temporal series and otic notch and bounded anteriorly by postorbital. Posteriorly, the squamosal articulates with the posterior elements of the palatal complex,...
(another small skull bone). And in mammals the quadrate and articular bones have become the incus
Incus
The incus or anvil is the anvil-shaped small bone or ossicle in themiddle ear. It connects the malleus to the stapes. It was first described by Alessandro Achillini of Bologna.The incus transmits sound vibrations from the malleus to the stapes....
and malleus
Malleus
The malleus or hammer is a hammer-shaped small bone or ossicle of the middle ear which connects with the incus and is attached to the inner surface of the eardrum...
bones in the middle ear.
Summary of the fossil evidence
Here is a very simplified "family tree" of the various lineages involved:--Tetrapod
Tetrapod
Tetrapods are vertebrate animals having four limbs. Amphibians, reptiles, birds and mammals are all tetrapods; even snakes and other limbless reptiles and amphibians are tetrapods by descent. The earliest tetrapods evolved from the lobe-finned fishes in the Devonian...
s------
| ("4 legged"; the earliest breathed via gills)
|
+-- Amphibian
Amphibian
Amphibians , are a class of vertebrate animals including animals such as toads, frogs, caecilians, and salamanders. They are characterized as non-amniote ectothermic tetrapods...
s ----------------------------------------------
|
`--------Reptiliomorph
Reptiliomorpha
Reptiliomorpha refers to an order or subclass of reptile-like amphibians, which gave rise to the amniotes in the Carboniferous. Under phylogenetic nomenclature, the Reptiliomorpha includes their amniote descendants though, even in phylogenetic nomenclature, the name is mostly used when referring to...
s-----
| ("reptile-like" amphibians)
|
`--Amniote
Amniote
The amniotes are a group of tetrapods that have a terrestrially adapted egg. They include synapsids and sauropsids , as well as their fossil ancestors. Amniote embryos, whether laid as eggs or carried by the female, are protected and aided by several extensive membranes...
s------
|
+--Sauropsids ("lizard faces")---------------
| (lizards, crocodilians, dinosaur
Dinosaur
Dinosaurs are a diverse group of animals of the clade and superorder Dinosauria. They were the dominant terrestrial vertebrates for over 160 million years, from the late Triassic period until the end of the Cretaceous , when the Cretaceous–Paleogene extinction event led to the extinction of...
s, birds
| Testudines; and some extinct groups)
|
`--Synapsid
Synapsid
Synapsids are a group of animals that includes mammals and everything more closely related to mammals than to other living amniotes. They are easily separated from other amniotes by having an opening low in the skull roof behind each eye, leaving a bony arch beneath each, accounting for their name...
s------
|
`--Pelycosaur
Pelycosaur
The pelycosaurs are an informal grouping composed of basal or primitive Late Paleozoic synapsid amniotes. Some species were quite large and could grow up to 3 meters or more, although most species were much smaller...
s----
|
`--Therapsids-----
|
`--Mammal
Mammal
Mammals are members of a class of air-breathing vertebrate animals characterised by the possession of endothermy, hair, three middle ear bones, and mammary glands functional in mothers with young...
s---------------
The first fully terrestrial vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
s were amniotes - their eggs had internal membranes which allowed the developing embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
to breathe but kept water in. This allowed amniotes to lay eggs on dry land, while amphibians generally need to lay their eggs in water. The first amniotes apparently arose in the late Carboniferous
Carboniferous
The Carboniferous is a geologic period and system that extends from the end of the Devonian Period, about 359.2 ± 2.5 Mya , to the beginning of the Permian Period, about 299.0 ± 0.8 Mya . The name is derived from the Latin word for coal, carbo. Carboniferous means "coal-bearing"...
from the ancestral reptiliomorph
Reptiliomorpha
Reptiliomorpha refers to an order or subclass of reptile-like amphibians, which gave rise to the amniotes in the Carboniferous. Under phylogenetic nomenclature, the Reptiliomorpha includes their amniote descendants though, even in phylogenetic nomenclature, the name is mostly used when referring to...
s (a group of amphibians whose only living descendants are amniotes). Within a few million years two important amniote lineages became distinct: mammals' synapsid
Synapsid
Synapsids are a group of animals that includes mammals and everything more closely related to mammals than to other living amniotes. They are easily separated from other amniotes by having an opening low in the skull roof behind each eye, leaving a bony arch beneath each, accounting for their name...
ancestors and the sauropsids, from which lizard
Lizard
Lizards are a widespread group of squamate reptiles, with nearly 3800 species, ranging across all continents except Antarctica as well as most oceanic island chains...
s, snake
Snake
Snakes are elongate, legless, carnivorous reptiles of the suborder Serpentes that can be distinguished from legless lizards by their lack of eyelids and external ears. Like all squamates, snakes are ectothermic, amniote vertebrates covered in overlapping scales...
s, crocodilians, dinosaur
Dinosaur
Dinosaurs are a diverse group of animals of the clade and superorder Dinosauria. They were the dominant terrestrial vertebrates for over 160 million years, from the late Triassic period until the end of the Cretaceous , when the Cretaceous–Paleogene extinction event led to the extinction of...
s and bird
Bird
Birds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...
s are descended.
The earliest known fossils of all these groups date from about 320 to 315M years ago. Unfortunately it is difficult to be sure about when each of them evolved, since vertebrate fossils from the late Carboniferous are very rare, and therefore the actual first occurrences of each of these types of animal might have been considerably earlier.
The pattern in most of the following sections is that each successive more "advanced" group started with the more "primitive" jaws and ears of its predecessors, then developed more mammal-like jaws and ears, and so on. The evolution of mammalian jaw joints and ears did not proceed neatly in step with the evolution of other mammalian features; or, to put it another way, all but the last of the various stages into which paleontologists divide the evolution towards the mammalian condition are not defined by their jaw joints and ears.
Early tetrapod and amniote ears
In modern amniotes (including mammals), the middle ear collects airborne sounds through an ear drum and transmits the vibrations to the inner ear via thin cartilaginous and ossified structures, which usually include the stapes (a stirrupStirrup
A stirrup is a light frame or ring that holds the foot of a rider, attached to the saddle by a strap, often called a stirrup leather. Stirrups are usually paired and are used to aid in mounting and as a support while using a riding animal...
-shaped auditory ossicle). But the earliest tetrapods, amphibians and amniotes probably did not have ear drums. In fact ear drums apparently evolved independently three to six times, in: stegocephalians (very primitive amphibians); in anurans (the amphibian group that includes frogs and toads); in synapsids (mammals and their extinct relatives), in diapsids (the most important sauropsid group, including lizards, crocodiles, dinosaurs and birds); perhaps separately in anapsids (turtles and their extinct relatives), if turtles are not modified diapsids; probably in seymouriamorphs
Seymouriamorpha
Seymouriamorpha were a small but widespread group of reptiliomorphs. Many seymouriamorphs were terrestrial or semi-aquatic. However, aquatic larvae bearing external gills and grooves from the lateral line system has been found, making them unquestionably amphibians. The adults were terrestrial...
(a group of reptiliomorphs); and possibly in some temnospondyls
Temnospondyli
Temnospondyli is a diverse order of small to giant tetrapods—often considered primitive amphibians—that flourished worldwide during the Carboniferous, Permian, and Triassic periods. A few species continued into the Cretaceous. Fossils have been found on every continent...
(primitive amphibians). In all basal members of the 3 major clades of amniotes (synapsids, eureptiles
Eureptilia
Eureptilia is one of the two major clades of the Sauropsida, the other being Anapsida . Eureptilia includes not only all Diapsids, but also a number of primitive Permo-Carboniferous forms previously classified under the Anapsida, in the old order "Cotylosauria".Primitive eureptilians were all...
, and parareptiles
Parareptilia
Parareptilia is a subclass or clade of reptiles which is variously defined as an extinct group of primitive anapsids, or a more cladistically correct alternative to Anapsida...
) 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. But there is increasing evidence that synapsids, eureptiles and parareptiles developed eardrums connected to the inner ear by stapes during the Permian
Permian
The PermianThe term "Permian" was introduced into geology in 1841 by Sir Sir R. I. Murchison, president of the Geological Society of London, who identified typical strata in extensive Russian explorations undertaken with Edouard de Verneuil; Murchison asserted in 1841 that he named his "Permian...
.
Early therapsid jaws and ears
The jaws of early synapsids, including the ancestors of mammals, were similar to those of other tetrapodTetrapod
Tetrapods are vertebrate animals having four limbs. Amphibians, reptiles, birds and mammals are all tetrapods; even snakes and other limbless reptiles and amphibians are tetrapods by descent. The earliest tetrapods evolved from the lobe-finned fishes in the Devonian...
s of the time, with a lower jaw consisting of a tooth
Tooth
Teeth are small, calcified, whitish structures found in the jaws of many vertebrates that are used to break down food. Some animals, particularly carnivores, also use teeth for hunting or for defensive purposes. The roots of teeth are embedded in the Mandible bone or the Maxillary bone and are...
-bearing dentary bone and several smaller posterior bones. The jaw joint consisted of the articular
Articular
The articular bone is part of the lower jaw of most tetrapods, including amphibians, sauropsids and early synapsids. In these animals it is connected to two other lower jaw bones, the suprangular and the angular...
bone in the lower jaw and the quadrate
Quadrate bone
The quadrate bone is part of a skull in most tetrapods, including amphibians, sauropsids , and early synapsids. In these animals it connects to the quadratojugal and squamosal in the skull, and forms part of the jaw joint .- Evolutionary variation :In snakes, the quadrate bone has become elongated...
in the upper jaw. The early pelycosaurs (late Carboniferous and early Permian) most probably did not have tympanic membranes (external eardrums), and their massive stapes bones supported the braincase, with the lower ends resting on the quadrates. But their descendants the therapsids (including mammals' ancestors) probably did have tympanic membranes and these probably were in contact with the quadrate bones; and the stapes bones were still in contact with the quadrates but functioned as auditory ossicles rather than braincase supports; so the therapsids' quadrates had a dual function, as part of the jaw joint and as parts of the hearing system.
Twin-jointed jaws
Permian
The PermianThe term "Permian" was introduced into geology in 1841 by Sir Sir R. I. Murchison, president of the Geological Society of London, who identified typical strata in extensive Russian explorations undertaken with Edouard de Verneuil; Murchison asserted in 1841 that he named his "Permian...
and early Triassic
Triassic
The Triassic is a geologic period and system that extends from about 250 to 200 Mya . As the first period of the Mesozoic Era, the Triassic follows the Permian and is followed by the Jurassic. Both the start and end of the Triassic are marked by major extinction events...
the dentary of therapsids, including the ancestors of mammals, continually enlarged while other jaw bones were reduced. Eventually, the dentary was able to make contact with the squamosal
Squamosal
The squamosal is a bone of the head of higher vertebrates. It is the principal component of the cheek region in the skull, lying below the temporal series and otic notch and bounded anteriorly by postorbital. Posteriorly, the squamosal articulates with the posterior elements of the palatal complex,...
, a bone in the upper jaw located anterior to the quadrate, allowing two simultaneous jaw joints - an anterior "mammal
Mammal
Mammals are members of a class of air-breathing vertebrate animals characterised by the possession of endothermy, hair, three middle ear bones, and mammary glands functional in mothers with young...
ian" 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 cynodont
Cynodont
Cynodontia or cynodonts are a taxon of therapsids which first appeared in the Late Permian and were eventually distributed throughout all seven continents by the Early Triassic . This clade includes modern mammals and their extinct close relatives. They were one of the most diverse groups of...
s and early mammaliforms
Mammaliaformes
Mammaliaformes is a clade that contains the mammals and their closest extinct relatives. Phylogenetically, it is defined as a clade including the most recent common ancestor of Sinoconodon, morganuconodonts, docodonts, Monotremata, Marsupialia, Placentalia, extinct members of this clade, and all...
. Morganucodon
Morganucodon
Morganucodon is an early mammalian genus which lived during the Late Triassic. It first appeared about 205 million years ago. This has also been identified with Eozostrodon. Unlike many other early mammals, Morganucodon is well represented by abundant and well preserved, though in the vast...
is one of the first discovered and most thoroughly studied of the mammaliforms, since an unusually large number of morganucodont fossils have been found, and
Morganucodon is an almost perfect intermediate in this respect (the "twin-jointed jaw") between the higher mammal-like reptiles on the one hand and the typical mammals on the other.(note: "mammal-like reptiles" is an obsolete term for the therapsids)
Mammal-like jaws and ears
As the dentary continued to enlarge during the Triassic, the older quadrate-articular joint fell out of use. Some of the bones were lost, but the quadrate (which is directly connected to the stapes), the articular (connected to the quadrate) and the angular (connected to the articular) became free-floating and associated with the stapes. This occurred at least twice in the mammaliformes ("almost-mammals"). The Multituberculates, which lived from about 160M years ago (mid-JurassicJurassic
The Jurassic is a geologic period and system that extends from about Mya to Mya, that is, from the end of the Triassic to the beginning of the Cretaceous. The Jurassic constitutes the middle period of the Mesozoic era, also known as the age of reptiles. The start of the period is marked by...
) to about 35M years ago (early Oligocene) had jaw joints that consisted of only the dentary and squamosal bones, and the quadrate and articular bones were part of the middle ear; but other features of their teeth, jaws and skulls are significantly different from those of mammals.
In the lineage most closely related to mammals, the jaws of Hadrocodium
Hadrocodium
Hadrocodium wui is an extinct basal mammal species that lived during the Lower Jurassic in what is now the Yunnan province of China...
(about 195M years ago in the very early Jurassic) suggest that it or a very close ancestor 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, and the absence of this trough which suggests that Hadrocodium’s ear was part of the cranium, as it is in mammals, and hence that the former articular and quadrate had migrated to the middle ear and become the malleus and incus; but Hadrocodium’s dentary has a "bay" at the rear which mammals lack, a hint that that its dentary bone retained the same shape that it would have had if the articular and quadrate had remained part of the jaw joint. It has been suggested that a relatively large trough in the jaw bone of the early Cretaceous monotreme
Monotreme
Monotremes are mammals that lay eggs instead of giving birth to live young like marsupials and placental mammals...
Teinolophos
Teinolophos
Teinolophos trusleri was a prehistoric species of monotreme, or egg-laying mammal. It is known from a lower jawbone found in Flat Rocks, Victoria, Australia. It lived during the Aptian age of the Lower Cretaceous. It is the earliest known relative of the Platypus.The species name honours the...
provides evidence of a pre-mammalian jaw joint, because therapsids and many mammaliforms had such troughs, in which the articular and angular bones "docked", and therefore that Teinolophos had a pre-mammalian middle ear; and therefore that the mammalian middle ear ossicles evolved indepedendently in monotremes and in other mammals. But a more recent analysis of Teinolophos concluded that the animal was a full-fledged platypus
Platypus
The platypus is a semi-aquatic mammal endemic to eastern Australia, including Tasmania. Together with the four species of echidna, it is one of the five extant species of monotremes, the only mammals that lay eggs instead of giving birth to live young...
and the trough was a channel for the large number of nerves that collect signals from the electrical and vibration sensors in the bill (this is a signature feature of the platypi within monotremes), and therefore that the trough is not evidence that Teinolophos had a pre-mammalian jaw joint and a pre-mammalian middle ear. Ironically Rich and Vickers-Rich were among the authors of the 2005 paper on which they later cast doubt.
A recently discovered intermediate form is the primitive mammal Yanoconodon
Yanoconodon
Yanoconodon is a monotypic genus of extinct early mammal whose representative species Yanoconodon allini lived 125 million years ago during the Mesozoic in what is now China. It is considered to be a transitional fossil due to the formation of its middle ear, which is a cross between those of...
, from 125 million years ago in the Mesozoic
Mesozoic
The Mesozoic era is an interval of geological time from about 250 million years ago to about 65 million years ago. It is often referred to as the age of reptiles because reptiles, namely dinosaurs, were the dominant terrestrial and marine vertebrates of the time...
, in which 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
Meckel's cartilage
The cartilaginous bar of the mandibular arch is formed by what are known as Meckel’s cartilages also known as Meckelian cartilages; above this the incus and malleus are developed....
, which in more advanced mammals dissolves during development.
How these changes affected hearing
The frequency rangeHearing (sense)
Hearing is the ability to perceive sound by detecting vibrations through an organ such as the ear. It is one of the traditional five senses...
and sensitivity of the ear
Ear
The ear is the organ that detects sound. It not only receives sound, but also aids in balance and body position. The ear is part of the auditory system....
is dependent upon the shape and arrangement of the middle-ear bones. In early synapsids such as the pelycosaurs, the quadrate and articular had to function as the jaw joint, and this severely limited how far these bones could be modified to alter the frequency range of the ear. But once these bones were no longer involved in the jaw joint, variations which affected hearing would not also affect jaw joint function, and this allowed unconstrained evolution of the mammalian hearing apparatus. By the Jurassic
Jurassic
The Jurassic is a geologic period and system that extends from about Mya to Mya, that is, from the end of the Triassic to the beginning of the Cretaceous. The Jurassic constitutes the middle period of the Mesozoic era, also known as the age of reptiles. The start of the period is marked by...
, the typical mammalian ear had evolved, in which the angular had become the tympanic annula (a bony support for the tympanic membrane), while the articular and quadrate had become the malleus
Malleus
The malleus or hammer is a hammer-shaped small bone or ossicle of the middle ear which connects with the incus and is attached to the inner surface of the eardrum...
and incus
Incus
The incus or anvil is the anvil-shaped small bone or ossicle in themiddle ear. It connects the malleus to the stapes. It was first described by Alessandro Achillini of Bologna.The incus transmits sound vibrations from the malleus to the stapes....
, respectively, connected in series with the stapes. This series of three bones acts as an amplification
Amplifier
Generally, an amplifier or simply amp, is a device for increasing the power of a signal.In popular use, the term usually describes an electronic amplifier, in which the input "signal" is usually a voltage or a current. In audio applications, amplifiers drive the loudspeakers used in PA systems to...
system to allow enhanced hearing.
The transition between these two states is one of the most well-documented and supported in all of evolution, and newly discovered fossils from this transitional period have recently improved our understanding of this transition. But they also suggest that it was not a simple linear process from the early therapsid jaw (quadrate-articular joint) and middle ear (with stapes as the only ossicles) to the modern mammalian condition.
Natural selection
It has been suggested that natural selectionNatural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
could be a factor in the preservation of the structure of the middle ear in mammals. Many of the earliest mammals were quite small, and the dentition indicates that they were insectivorous. If they were "warm-blooded
Warm-blooded
The term warm-blooded is a colloquial term to describe animal species which have a relatively higher blood temperature, and maintain thermal homeostasis primarily through internal metabolic processes...
" (endothermic), like modern mammals, then they could have been nocturnal. This fits with the popular image of small, nocturnal insectivorous mammals surviving in niches not accessible to the large, dominant contemporary dinosaurs. The enhanced hearing, particularly in the higher frequencies, would be helpful for nocturnal animals, in particular for detecting insects. This scenario is consistent with selective advantage being a contributory factor to the transition.
Summary
While the stapes is present in many types of tetrapods, the addition of the incus and malleus (also known as quadrate and articular) in the middle ear is a signature feature of mammals, distinguishing them from reptiles and all other vertebrates. They therefore have the appearance of representing a discontinuity in the tree of life. But in the early 19th century, it was hypothesized that these bones are not a total novelty, but are the equivalents of two bones which non-mammals have in their jaws. This hypothesis made sense, not only of the existence of these middle-ear bones, but also of certain other features of the anatomy, such as the paths taken by nerves in the head.As evolutionary biology began to be expanded upon, this relationship became treated as one of common descent. For the evolutionary explanation to make sense, it seemed to demand that there would be a transition in function between being part of the feeding mechanism in the joint of the jaw and serving only in hearing; and this would mean that somehow there had to be an intermediate connecting these two quite different functions. With the discovery of Morganucodon and other fossils, there were concrete examples of this. There was a double jaw joint: the "older reptilian", as well as the "newer mammalian", in the same animal. This meant a confirmation of the pattern of inference from comparative anatomy to evolutionary biology.
The earliest mammals were generally small animals, probably nocturnal insectivores. This suggests a plausible evolutionary mechanism driving the change, for 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. Natural selection would account for the success of this feature. And still one more connection with another part of biology: genetics suggested a mechanism for this transition, the kind of major change of function seen elsewhere in the world of life being studied by Evodevo.
See also
- Evolution of mammalsEvolution of mammals__FORCETOC__The evolution of mammals within the synapsid lineage was a gradual process that took approximately 70 million years, beginning in the mid-Permian. By the mid-Triassic, there were many species that looked like mammals, and the first true mammals appeared in the early Jurassic...
- MorganucodonMorganucodonMorganucodon is an early mammalian genus which lived during the Late Triassic. It first appeared about 205 million years ago. This has also been identified with Eozostrodon. Unlike many other early mammals, Morganucodon is well represented by abundant and well preserved, though in the vast...
- Maotherium asiaticus
- OligokyphusOligokyphusOligokyphus was an advanced herbivorous cynodont of the late Triassic to early Jurassic periods. Originally considered to be an early mammal, it is now classified as a synapsid because Oligokyphus does not have the mammalian jaw attachments and it retains a vestigial joint between the quadrate...
- ProbainognathusProbainognathusProbainognathus is a genus of meat-eating mammal-like reptile that lived during the lower Upper Triassic of South America. This creature had an incipient squamosal-dentary jaw-cranium joint, which is a clearly mammalian anatomical feature. It was at the very least closely related to the family of...
- Transitional fossilTransitional fossilA transitional fossil is any fossilized remains of a lifeform that exhibits characteristics of two distinct taxonomic groups. A transitional fossil is the fossil of an organism near the branching point where major individual lineages diverge...
- YanoconodonYanoconodonYanoconodon is a monotypic genus of extinct early mammal whose representative species Yanoconodon allini lived 125 million years ago during the Mesozoic in what is now China. It is considered to be a transitional fossil due to the formation of its middle ear, which is a cross between those of...