Evolution of mammalian auditory ossicles

The evolution of mammalian auditory ossicles was an evolutionary event 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 purpose 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.

History

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.

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 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]

Phylogeny

The following simplified cladogram displays relationships between tetrapods:

Tetrapods	Amphibians   Reptiliomorphs Amniotes Sauropsids   Synapsids other synapsids   Eupelycosaurs   other eupelycosaurs   Therapsids   other therapsids     Mammals

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 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]

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

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][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 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]

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][38]

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.[39] 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.[40][41] Researchers now hypothesize that the definitive mammalian middle ear did not emerge any earlier than the late Jurassic (~163M years ago).[41]

Teinolophos

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". Thus, Teinolophos had a pre-mammalian middle ear, indicating that the mammalian middle ear ossicles evolved independently in monotremes and in other mammals.[42] 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.[43]

Yanoconodon

A recently discovered intermediate form is the primitive mammal Yanoconodon, which lived approximately 125 million years ago in the Mesozoic era. 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. [44][41] 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.[45]

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

See also

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

References

1. Allin EF (December 1975). "Evolution of the mammalian middle ear". Journal of Morphology. 147 (4): 403–437. doi:10.1002/jmor.1051470404. PMID 1202224.
2. Meier & Ruf (2016), page 270, Introduction, "The study of the mammalian middle ear has been one of the central themes of vertebrate morphological research of the last 200 years."
3. Cuffey CA (2001). "The Fossil Record: Evolution or "Scientific Creation": Mammal-Like Reptiles". GCSSEPM Foundation. Archived from the original on May 1, 2009. Retrieved 2009-06-17.
4. "Jaws to ears in the ancestors of mammals". UC Berkeley. Retrieved 20 January 2018.
5. Maier W, Ruf I (February 2016). "Evolution of the mammalian middle ear: a historical review". Journal of Anatomy. 228 (2): 270–83. doi:10.1111/joa.12379. PMC 4718169. PMID 26397963.
6. Gaupp E. "Zur Entwickelungsgeschichte und vergleichen Morphologie des Schädels von Echidna aculeata var. ehenden typical" [On the developmental history and comparative morphology of the skull of Echidna aculeata var. typical]. Richard Semon Fortschungsreisen (in German). 3: 539–788.
7. Takechi M, Kuratani S (2010). "History of Studies on Mammalian Middle Ear Evolution: A Comparative Morphological and Developmental Biology Perspective". Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 314B (6): 417–433. doi:10.1002/jez.b.21347.
8. Appel TA (1987). The Cuvier–Geoffroy Debate: French Biology in the Decades before Darwin. New York and Oxford: Oxford University Press. pp. 206–207. ISBN 0-19-504138-0.
9. Novacek MJ (1993). Hall BK, Hanken J (eds.). The Skull. Chicago: University of Chicago Press. pp. 438–545. ISBN 0-226-31568-1. Novacek references these early works: Meckel JF (1820). Handbuch der Menschlichen Anatomie [Handbook of Human Anatomy] (in German). Halle. – Reichert KB (1837). "Ueber die Visceralbogen der Wirbelthiere im Allegemeinen und deren Metamorphosen bei den Vögln und Säugethieren" [On the visceral arches of the vertebrates in general and their metamorphoses among the birds and mammals]. Archiv für Anatomie, Physiologie, und wissenschaftliche Medizin (in German). Leipzig: 120–122. – Gaupp E (1913). "Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage)" [The Reichert theory (question of the hammer, anvil and stirrup)]. Archiv für Anatomie und Entwicklungsgeschichte (in German): 1–416.
10. Goodrich ES (1958) [1934]. Studies on the Structure and Development of Vertebrates. Dover. p. 474.
11. Crompton AW, Jenkins FA (1973). "Mammals from Reptiles: A Review of Mammalian Origins". Annual Review of Earth and Planetary Sciences. 1: 131–155. Bibcode:1973AREPS...1..131C. doi:10.1146/annurev.ea.01.050173.001023.
12. Kühne WG (1958). "Rhaetische Triconodonten aus Glamorgan, ihre Stellung zwischen den Klassen Reptilia und Mammalia und ihre Bedeutung für die REICHART'sche Theorie" [Rhaetic triconodonts from Glamorgen, their place between the Reptilia and Mammalia classes and their meaning for the Reichart theory]. Paläontologische Zeitschrift (in German). 32 (3/4): 197–235. doi:10.1007/BF02989032.
13. Gilbert SF (2003). Developmental biology (7th ed.). Sunderland, Mass: Sinauer Associates. p. 435. ISBN 0-87893-258-5.
14. Mallo M (March 2001). "Formation of the middle ear: recent progress on the developmental and molecular mechanisms". Developmental Biology. 231 (2): 410–419. doi:10.1006/dbio.2001.0154. PMID 11237469.
15. Raff RA (December 2007). "Written in stone: fossils, genes and evo-devo". Nature Reviews Genetics. 8 (12): 911–920. doi:10.1038/nrg2225. PMID 18007648.
16. Wilson J, Tucker AS (February 2004). "Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint". Developmental Biology. 266 (1): 138–150. doi:10.1016/j.ydbio.2003.10.012. PMID 14729484.
17. Tucker AS, Watson RP, Lettice LA, Yamada G, Hill RE (March 2004). "Bapx1 regulates patterning in the middle ear: altered regulatory role in the transition from the proximal jaw during vertebrate evolution". Development. 131 (6): 1235–1245. doi:10.1242/dev.01017. PMID 14973294.
18. A survey of the genes involved in the development of the vertebrate middle ear is given in Chapman SC (January 2011). "Can you hear me now? Understanding vertebrate middle ear development". Frontiers in Bioscience. 16 (2): 1675–92. doi:10.2741/3813. PMC 3065862. PMID 21196256.
19. Sienknecht UJ (July 2013). "Developmental origin and fate of middle ear structures". Hearing Research. 301: 19–26. doi:10.1016/j.heares.2013.01.019.
20. White T. "Unit 430: Mammalia: Overview". PALAEOS: The Trace of Life on Earth. palaeos.com. Archived from the original on June 15, 2008. Retrieved 2008-07-21.
21. Cowen R (2000). History of life. Oxford: Blackwell Science. p. 432. ISBN 0-632-04444-6.
22. Masali M (October 1992). "The ear ossicles and the evolution of the primate ear: A biomechanical approach". Human Evolution. Springer Netherlands. 7 (4): 1–5. doi:10.1007/BF02436407.
23. White T. "Amniota". PALAEOS: The Trace of Life on Earth. palaeos.com. Retrieved 2008-07-21.
24. Theobald D (2004). "29+ Evidences for Macroevolution: Part 1, Example 2: reptile-mammals". TalkOrigins. Retrieved 2009-06-17.
25. Laurin M (January–March 1998). "The importance of global parsimony and historical bias in understanding tetrapod evolution. Part I. Systematics, middle ear evolution and jaw suspension". Annales des Sciences Naturelles - Zoologie et Biologie Animale. 19 (1): 1–42. doi:10.1016/S0003-4339(98)80132-9.
26. Laurin M. "Hearing in Stegocephalians". Tree of Life. Tree of Life Project. Retrieved 2008-07-21.
27. Müller J, Tsuji LA (2007). "Impedance-matching hearing in Paleozoic reptiles: evidence of advanced sensory perception at an early stage of amniote evolution". PLoS ONE. 2 (9): e889. Bibcode:2007PLoSO...2..889M. doi:10.1371/journal.pone.0000889. PMC 1964539. PMID 17849018.
28. Fay RR, Manley GA, Popper AN (2004). Evolution of the vertebrate auditory system. Berlin: Springer. ISBN 0-387-21089-X.
29. Luo ZX (December 2007). "Transformation and diversification in early mammal evolution" (PDF). Nature. 450 (7172): 1011–1019. Bibcode:2007Natur.450.1011L. doi:10.1038/nature06277. PMID 18075580. Archived from the original (PDF) on November 27, 2012.
30. Sidor CA (July 2001). "Simplification as a trend in synapsid cranial evolution". Evolution. 55 (7): 1419–42. doi:10.1554/0014-3820(2001)055[1419:saatis]2.0.co;2. PMID 11525465.
31. Benton MJ (1990). Vertebrate palaeontology : biology and evolution. Unwin Hyman. p. 229. ISBN 0-04-566001-8.
32. Colbert E (1991). Evolution of the vertebrates : a history of the backboned animals through time. New York: Wiley-Liss. p. 228. ISBN 0-471-85074-8.
33. Kermack KA, Mussett F, Rigney HW (January 1981). "The skull of Morganucodon". Zoological Journal of the Linnean Society. Linnaean Society of London. 71 (1): 1–158. doi:10.1111/j.1096-3642.1981.tb01127.x.
34. Biello D (2007-03-14). "From Jaw to Ear: Transition Fossil Reveals Ear Evolution in Action". Scientific American. Retrieved 2009-06-17. Now hear this: early mammal fossil shows how sensitive ear bones evolved
35. Bowler PJ (1996). "Chapter 6: The Origin of Birds and Mammals". Life's splendid drama: evolutionary biology and the reconstruction of life's ancestry, 1860-1940. University of Chicago Press. ISBN 0-226-06921-4.
36. Janvier P (2002). Early vertebrates. Oxford Monographs on Geology and Geophysics, 33. Clarendon Press. p. 56. ISBN 978-0-19-852646-9.
37. Zimmer C (15 October 2008). "The Shoulder Bone's Connected to the Ear Bone…". Discover.
38. White T. "Mammaliformes". PALAEOS: The Trace of Life on Earth. palaeos.com. Archived from the original on June 4, 2008. Retrieved 2008-07-21.
39. White T. "Symmetrodonta". PALAEOS: The Trace of Life on Earth. palaeos.com. Archived from the original on July 3, 2008. Retrieved 2008-07-21.
40. Wang, Y; Hu, Y; Meng, J; Li, C (2001). "An Ossified Meckel's Cartilage in Two Cretaceous Mammals and Origin of the Mammalian Middle Ear". Science. 294 (5541): 357–361. Bibcode:2001Sci...294..357W. doi:10.1126/science.1063830. ISSN 0036-8075. PMID 11598297.
41. Ramírez-Chaves HE, Weisbecker V, Wroe S, Phillips MJ (2016). "Resolving the evolution of the mammalian middle ear using Bayesian inference". Frontiers in Zoology. 13 (1): 39. doi:10.1186/s12983-016-0171-z. PMC 4997658. PMID 27563341.
42. Rich TH, Hopson JA, Musser AM, Flannery TF, Vickers-Rich P (February 2005). "Independent origins of middle ear bones in monotremes and therians". Science. 307 (5711): 910–914. Bibcode:2005Sci...307..910R. doi:10.1126/science.1105717. PMID 15705848.
43. Rowe T, Rich TH, Vickers-Rich P, Springer M, Woodburne MO (January 2008). "The oldest platypus and its bearing on divergence timing of the platypus and echidna clades". Proceedings of the National Academy of Sciences of the United States of America. 105 (4): 1238–1242. Bibcode:2008PNAS..105.1238R. doi:10.1073/pnas.0706385105. PMC 2234122. PMID 18216270.
44. Myers PZ (March 16, 2007). "Yanoconodon, a transitional fossil". Pharyngula: Evolution, development, and random biological ejaculations from a godless liberal.
45. Meng, J; Wang, Y; Li, C (April 2011). "Transitional mammalian middle ear from a new Cretaceous jehol eutriconodont". Nature. 472 (7342): 181–185. Bibcode:2011Natur.472..181M. doi:10.1038/nature09921. PMID 21490668.
46. Köppl C (11 August 2009). "Evolution of sound localization in land vertebrates". Current Biology. 19 (15): R635–R639. doi:10.1016/j.cub.2009.05.035. PMID 19674542.

Further reading

• Allin EF, Hopson JA (1992). "Chapter 28: Evolution of the Auditory System in Synapsida ("Mammal-Like Reptiles" and Primitive Mammals) as Seen in the Fossil Record". In Popper AN, Webster DB, Fay RR (eds.). The Evolutionary biology of hearing. Berlin: Springer-Verlag. pp. 587–614. ISBN 0-387-97588-8.
• Anthwal N, Joshi L, Tucker AS (2013). "Evolution of the mammalian middle ear and jaw: adaptations and novel structures". Journal of Anatomy. 222 (1): 147–60. doi:10.1111/j.1469-7580.2012.01526.x. PMC 3552421. PMID 22686855.
• Arthur W (2011). "10.3 Compound Repatterning at a Single Level of Organisation". Evolution: A developmental approach. Oxford: Wiley-Blackwell. pp. 151–155. ISBN 978-1-4051-8658-2.
• Asher RJ (2012). Evolution and belief: confessions of a religious paleontologist. Cambridge & New York: Cambridge University Press. pp. 93–110, 196–200. ISBN 9780521193832.
• Gould SJ (1993). "Chapter 6: An Earful of Jaw". Eight Little Piggies: reflections in natural history. New York: Norton. ISBN 0-393-03416-X.
• Hopson JA (January 1987). "The mammal-like reptiles: a study of transitional fossils". The American Biology Teacher. 49 (1): 16–26. doi:10.2307/4448410. JSTOR 4448410.
• Kielan-Jaworowska Z (2013). "5. Origins of Mammals and the Earliest Representatives of Mammaliforms and Mammals". In Pursuit of Early Mammals. Life of the Past. Bloomington, Indiana: Indiana University Press. pp. 73–96. ISBN 978-0-253-00824-4. especially pages 85–96
• Luo ZX, Kielan-Jaworowska Z, Cifelli RL (2004). "Chapter 3: Origin of mammals". Mammals from the age of dinosaurs: origins, evolution, and structure. New York: Columbia University Press. ISBN 0-231-11918-6.
• Luo Z (2011). "Developmental Patterns in Mesozoic Evolution of Mammal Ears". Annual Review of Ecology, Evolution, and Systematics. 42: 355–380. doi:10.1146/annurev-ecolsys-032511-142302.
• Manley GA, Sienknecht UJ (2013). "Chapter 2: The Evolution and Development of Middle Ears in Land Vertebrates". In Puria S, Fay RR, Popper AN (eds.). The Middle Ear: Science, Otosurgery, and Technology. Springer Handbook of Auditory Research. 46. New York: Springer. pp. 7–30. doi:10.1007/978-1-4614-6591-1_2. ISBN 978-1-4614-6590-4.
• Meng J, Zheng XT, Wang XL (2016). "Ear Ossicle Morphology of the Jurassic Euharamiyidan Arboroharamiya and Evolution of Mammalian Middle Ear". Journal of Morphology. 279 (4): 441–457. doi:10.1002/jmor.20565. PMID 27228358. contains wide bibliography of scientific literature up to 2016
• Aitor Navarro‐Díaz; Borja Esteve‐Altava; Diego Rasskin‐Gutman (2019). "Disconnecting bones within the jaw‐otic network modules underlies mammalian middle ear evolution". Journal of Anatomy. in press. doi:10.1111/joa.12992. hdl:10261/206465. PMID 30977522.
• Rosowski JJ (1992). "Chapter 29: Hearing in Transitional Mammals: Predictions from the Middle-Ear Anatomy and Hearing Capabilities of Extant Mammals". In Popper AN, Webster DB, Fay RR (eds.). The Evolutionary biology of hearing. Berlin: Springer-Verlag. pp. 615–632. ISBN 0-387-97588-8.
• Rougier GW, White JR (2006). "Chapter 6: Major Changes in the Ear Region and Basicranium of Early Mammals". In Carrano MT, Gaudin TJ, Blob RW, Wible JR (eds.). Amniote paleobiology: perspectives on the evolution of mammals, birds, and reptiles: a volume honoring James Allen Hopson. Chicago: University of Chicago Press. pp. 269–311. ISBN 0-226-09477-4.
• Shubin N (2008). "Chapter 10: Ears". Your inner fish: a journey into the 3.5-billion-year history of the human body. New York: Pantheon Books. ISBN 978-0-375-42447-2.
• Tucker AS (2017). "Major evolutionary transitions and innovations: the tympanic middle ear". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 372 (1713): 20150483. doi:10.1098/rstb.2015.0483. PMC 5182415. PMID 27994124.

External links

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