Evolution of the mammalian middle ear: a historical review

Abstract

Here we present a brief, historical review of research into the mammalian middle ear structures. Most of their essential homologies were established by embryologists, notably including Reichert, during the 19th century. The evolutionary dimension was confirmed by finds of fossil synapsids, mainly from the Karroo of South Africa. In 1913, Ernst Gaupp was the first to present a synthesis of the available embryological and paleontological data, but a number of morphological details remained to be solved, such as the origin of the tympanic membrane. Gaupp favoured an independent origin of the eardrum in anurans, sauropsids, and mammals; we support most of his ideas. The present review emphasizes the problem of how the mammalian middle ear structures that developed at the angle of the lower jaw were transferred to the basicranium; the ontogenesis of extant marsupials provides important information on this question.

Keywords: Mammalia; evolution; middle ear; middle ear ossicles; ontogeny.

Figure 1

The theory of Reichert. (A) The interpretation by Gaupp (1913: his fig. 144, modified). The primary jaw articulation between quadrate and articular as seen in a schematic juvenile squamate (left side) representing (according to him) the ancestral morphotype; in fact, the quadrate articulates not only with the squamosal but also with the parotic process of the otic capsule lying underneath. The generalized mammalian condition is shown on the right side; homologues are given in the same coloration. Quadrate and articular have evolved into incus and malleus; at least proximal parts of the columella are homologous to the stapes. The primary jaw articulation corresponds to the incudo‐mallear joint, and a secondary jaw joint is formed between the dermal squamosal and dentary; the ectotympanic ring, which provides the frame for the tympanic membrane, is derived from the angular bone. This transition is very well documented in the fossil record. (B) The interpretation of Goodrich (1915); his slightly modified text Fig. 2 is labeled anew to make comparison with the figure of Gaupp easier. Goodrich assumed that the tympanic membrane is homologous in sauropsids and mammals.

Figure 2

Reconstructed recessus mandibularis (tympanic cavity) in primitive therocephalian therapsids. Above is the skull of Glanosuchus macrops, a scymnosaurine therocephalian (modified from Brink, 1988). Below are four cross‐sections of Glanosuchus sp. drawn from a grinding series housed at the Department of Zoology at the University of Stellenbosch: the section planes are indicated by the stippled lines in the figure of the skull of Glanosuchus as well as by letters A–D. The likely position of Meckel's cartilage is indicated by a dotted line, i.e. it was formed as cartilage; only its posterior end is ossified as articular. In the cross‐sections the hypothetical recessus mandibularis is drawn in by a stippled contour underneath the very thin bony plate of the reflected lamina of the angular. The proximal portions of the hyoids show the mammalian tympanohyal (from Maier & van den Heever, 2002).

Figure 3

Evolutionary and ontogenetic development of the mammalian middle ear ossicles. (A) Comparison of the skull of a neonatal marsupial (Monodelphis domestica; above) and a basal amniote (below). The exocranium (brown) of the basal amniote is adopted from Captorhinus, and it is combined with a hypothetical ‘reptilian’ endocranium of a fetal stage (blue = neural endocranium, purple = viscerocranium, yellow = hyobranchial skeleton). The hyostylic suspension of the jaws in the basal amniote already shows the future arrangement of the ear ossicles: articular and quadrate (which will become malleus and incus, respectively) forming the primary jaw joint, and hyomandibula (which will become the stapes) inserted into the fenestra ovalis of the otic capsule. Neonatal marsupials retain the primary jaw articulation and the elements of the secondary joint (dentary and squamosal more densely stained) lie still far apart; both are gradually approaching each other in phylogeny and ontogeny, and finally develop an ‘Anlagerungsgelenk’ (‘appositional joint’); the red circle in the basal amniote indicates the future position of the tympanic membrane at the angle of the lower jaw, the yellow circle that of the future tympanic membrane behind the quadrate in squamates (adopted from Maier & Werneburg, 2014). (B) Evolutionary series of fossil synapsids (Dimetrodon, Thrinaxodon, Morganucodon) and postnatal stage of Monodelphis showing the gradual transformation of the angle of the lower jaw into sound‐transmitting middle ear structures (modified from Allin, 1975; and Maier, 1990: medial view on the left, lateral view on the right). (C) Postnatal ontogeny of Monodelphis demonstrating the translocation of the ectotympanic (red colour) from the lower jaw to the skull base (modified from Maier, 1990; adult stage in posterior view, early postnatal stages as cross‐sections). (D) Close‐up of the jaw and ear region in a 7‐day‐old Monodelphis, resembling that of Triassic cynodonts (lateral view; modified from Maier, 1990). (E) Posterior view of the ear region of Morganucodon from the Triassic‐Jurassic boundary, showing that the quadrate and articular elements of the primary jaw joint are functionally replaced by the squamosal and dentary of the secondary articulation (which is more laterally positioned). The primary elements are transformed into incus and malleus, but they are still attached to the lower jaw (modified from Kermack et al. 1981). The hatched arrows indicate that the middle ear structures of the adult marsupial are reached by two pathways: the phylogenetic and the ontogenetic.