Major evolutionary transitions and innovations: the tympanic middle ear

Abstract

One of the most amazing transitions and innovations during the evolution of mammals was the formation of a novel jaw joint and the incorporation of the original jaw joint into the middle ear to create the unique mammalian three bone/ossicle ear. In this review, we look at the key steps that led to this change and other unusual features of the middle ear and how developmental biology has been providing an understanding of the mechanisms involved. This starts with an overview of the tympanic (air-filled) middle ear, and how the ear drum (tympanic membrane) and the cavity itself form during development in amniotes. This is followed by an investigation of how the ear is connected to the pharynx and the relationship of the ear to the bony bulla in which it sits. Finally, the novel mammalian jaw joint and versatile dentary bone will be discussed with respect to evolution of the mammalian middle ear.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

Keywords: bulla; jaw joint; mammal evolution; middle ear; tympanic membrane.

Figure 1.

Anatomy of the middle ear. (a) Schematic of a sauropsid (bird, lizard) middle ear with a single ossicle spanning the middle ear cavity. (b) Schematic of a mammalian middle ear with three ossicles in a chain within the cavity. Origin of ossicles: Light blue denotes first arch neural crest derived tissue. Dark blue denotes second arch neural crest derived tissue. Red denotes mesoderm-derived tissue (stapes footplate). S, stapes; M, malleus; I, incus; MEC, middle ear cavity.

Figure 2.

Cavitation of the ear. (a–c) Proposed processes of creating an air-filled space. (a) Invasion of the endoderm as a sheet of tissue wrapping around the ossicles. (b) Break of the endoderm to allow the tissue to move around the ossicles. (c) No invasion of the endoderm but creation of a cavity by retraction and transformation of the mesenchyme. (d) Process based on lineage tracing showing a dual origin of the middle ear lining incorporating some of the ideas from the previous three models. (e–g) Histology sections through the middle ear during retraction of the mesenchyme: (e) mouse E18.5; (f) shrew P5; (g) postnatal opossum. Arrows represent the mesenchyme retracting back from the forming tympanic membrane creating a cavity.

Figure 3.

Atympanic ears. (a) Bearded dragon (Pogona viviceps) with superficial tympanic membrane. Inset shows ossicle visible through the membrane. (b) Chameleon (Chamaeleo calyptratus) showing lack of an external ear canal. (c) Skeletal prep of a newborn corn snake (Elaphe guttata), with the position of the stapes outlined (white dots). (d) Faxitron of adult corn snake. Arrow points to the thin stapes, which is connected to the quadrate. (e) Sphenodon punctatus approximately eight months incubation. The stapes is inserted into the otic capsule on one side and into a fibrous sheath (arrowhead) on the other. The middle ear cavity has not extended up past the stapes, which is still surrounded by mesenchyme. Sphenodon slides from Denby collection at KCL. Q, quadrate; A, articular; S, stapes; PTT, pharyngotympanic tube (connecting ear and pharynx).

Figure 4.

Connection to the pharynx. (a) Frontal section through the Eustachian tube (ET) in a mouse P22. The narrow ET connects the middle ear (out of plane of section) to the naso-pharynx (P). The tube is supported by cartilage (arrows) and is lined with mucin-producing cells (stained blue). (b) Frontal section through a gecko embryo. The middle ear cavity (MC) is connected to the pharynx (P) via a wide tube, the pharyngotympanic tube (PTT).

Figure 5.

The novel mammalian jaw joint. (a) Histology section through a weaning mouse showing the condylar cartilage (C), disc (D) and glenoid fossa (GF). (b) MicroCT of the condyle sitting in the glenoid fossa in an adult mouse. (c) Skeletal prep of adult shrew dentary with large coronoid. (d) Skeletal prep of adult guinea pig dentary with almost complete loss of the coronoid. Asterisks indicate condyle; arrows point to coronoids.