Evolution of the Mammalian Middle Ear EDGAR F ALLIN Deprr rtmen t of Antitomy, U n i v e i s i t y of’ Wrsc o i i s i n , Mir d i s o n , Wisronsin 53706 I

ABSTRACT The structure and evolution of the mandible, suspensorium, and stapes of mammal-like reptiles and early mammals are examined i n an attempt to determine how, why, and when in phylogeny the precursors of the mammalian tympanic bone, malleus, and incus (postdentary jaw elements and quadrate) came to function i n the reception of air-borne sound. The following conclusions are reached: It is possible that at no stage in mammalian phylogeny was there a middle ear similar to that of “typical” living reptiles, with a postquadrate tympanic membrane contacted by an extrastapes. The squamosal sulcus of cynodonts and other therapsids, usually thought to have housed a long external acoustic meatus, possibly held a depressor mandibulae muscle. In therapsids a n air-filled chamber (recessus mandibularis of Westoll) extended deep to the reflected lamina and into the depression (external fossa) on the outer aspect of the angular element. A similar chamber was present in sphenacodontids but pterygoideus musculature occupied the small external fossa. The thin tissues superficial to the recessus mandibularis served as eardrum. Primitively, vibrations reached the stapes mainly via the anterior hyoid cornu, but in dicynodonts, therocephalians, and cynodonts, vibrations passed mainly or exclusively from mandible to quadrate to stapes and the reflected lamina was a component of the eardrum. In the therapsid phase of mammalian phylogeny, auditory adaptation was a n important aspect of jaw evolution. Auditory efficiency, and sensitivity to higher sound frequencies, were enhanced by diminution and loosening of the postdentary elements and quadrate, along with transference of musculature from postdentary elements to the dentary. These changes were made possible by associated modifications, including posterior expansion of the dentary. Establishment of a dentray-squamosal articulation permitted continuation of these trends, leading to the definitive mammalian condition, with no major change in auditory mechanism except that in most mammals (not monotremes) the angular, as tympanic, eventually became a non-vibrating structure.

One of the most remarkable evolutionary events was the transformation of ancestral jaw elements (angular, articular, and quadrate) into the tympanic, malleus, and incus of the mammalian middle ear. Paleontological evidence bearing on this transformation is now extensive, permitting inquiry into the underlying causes. For this, it is necessary to reconstruct relevant soft tissues and to deduce function from morphology. Examination of the fossil evidence has led me to question the following widely favored reconstructions and functional interpretations (Hopson, ’66): 1. The reptilian progenitors of mammals possessed a middle ear essentially like that of “typical” living reptiles, with a tympanic J. MORPH., 147: 40-38.

membrane behind the quadrate, contacted by the columella. 2. Cynodonts, the group of reptiles immediately ancestral to the Mammalia, had a long, tubular external acoustic meatus. 3. The modifications in jaw structure in cynodonts and their ancestors (including enlargement of the dentary element, reduction and loosening of the postdentary elements and quadrate, restructuring of all these parts, and shifting of jaw musculature onto the dentary) took place for mechanical reasons having little or nothing to do with sound reception. 4. The same holds for at least the initial 1 Present address: Department of Anatomy, University of Illinois, P.O. Box 6998, Chicago, Illinois 60680.

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stages of replacement of the reptilian (articular-quadrate) jaw point by the mammalian (dentary-squamosal or temporomandibular) articulation. 5. Jaw components first began to be set into perceptible vibration by air-borne sound after, or shortly before, formation of the dentary-squamosal articulation. 6. At no stage was the angular element, or the derived tympanic (ectotympanic), set into perceptible vibration by aerial sound. This paper is an attempt to integrate existing and new information into a comprehensive hypothesis to explain this extraordinary structural transfiguration in functional (adaptational) terms. MATERIALS

Through the courtesy of Prof. A. W. Crompton and the late Prof. A. S. Romer, I was able to examine fossil specimens and use facilities in the Museum of Comparative Zoology, Harvard University (abbreviated MCZ in catalogue labels cited). These were various labyrinthodont amphibians, Captorhinus, several pelycosaurs, the dicynodont Dinodontosaurus, and many cynodonts including Exaeretodon, Massetognathus, Probelesodon, Probainognathus, Diademodon (cast), Thrinaxodon and Trirachodon, as well as the Rhaetic mammals Megazostrodon and Eozostrodon (several mandibles from the collection of Prof. F. R. Parrington). I also studied Prof. Crompton’s many stereophotographs of dicynodonts, a pristerognathid therocephalian, a galesaurid cynodont, tritheledonts, Oligokyphus and other tritylodonts. At the Smithsonian Institute I examined dicynodonts through the courtesy of Dr. N. Hotton, 111. Prof. J. A. Hopson made available specimens of Bauria, Bienotherium, the sectioned skull and jaw of a galesaurid (cynodont B of Olson, ’44), casts of the stapes and adjacent parts of Scatendon and the articular region of the mandible of Cynognathus, as well as skulls of the presentday iguana and the monotreme Urnithorhynchus (with ear ossicles and hyoid apparatus). Prof. H. R. Barghusen provided skulls of various present-day reptiles, casts of the quadrate complex of Dimetrodon and two gorgonopsians, and stereophotographs of the captorhinomorph Protorothyris.

Additional skulls of modern mammals, birds, and reptiles, including an “exploded alligator skull and mandible, were examined in the Osteology Museum, University of Wisconsin, Madison, and the Field Museum of Natural History, Chicago. Reconstructions of developing human middle ear structures were available to me in the local Wisconsin Ear Collection. Dissections were performed on two formalin-perfused heads of the lizard Tupinambis teguixin provided by Dr. W. L. R. Cruce and on the middle ear of an American opossum provided by Prof. H. W. Mossman. OBSERVATIONS AND DISCUSSION

T h e middle ear of living mammals Three endochrondral bones, the malleus, incus, and stapes, linked by synovial joints and suspended in an air-filled chamber (the cavum tympani), transmit vibrations from the tympanic membrane to the fenestra vestibuli (fig. 1). The malleus bears an anterior process, and a manubrium which projects across the externally concave eardrum to its center. The incus has a posterior process (crus brevis) bonded by ligament to the petrosal bone and a stapedial process (crus longus) projecting downward to articulate with the stapes. The expanded footplate of the stapes occupies the fenestra vestibuli (ovalis). The tympanic apparatus (drum, cavum tympani, and ossicles) converts the pressure waves of air-borne sound into oscillating displacements and matches the acoustic impedance of air with the higher impedance of the cochlear liquid. This impedance-matching (transformer) function is accomplished by the concentration of sound energy from the large tympanic membrane to the small stapedial footplate and, less importantly, by the ossicular lever system (fig. 1). The ossicles vibrate about an axis passing through the posterior process of the incus and the anterior process of the malleus. The force arm to the center of the drum exceeds the resistance arm to the stapes, providing a mechanical advantage. Multiplication of the lever ratio by the drum-footplate (“hydraulic”) ratio gives the total transformer ratio (Webster, ’66). The tympanic (ectotympanic) bone supports the eardrum. In the fetus it is a ioosely suspended incomplete ring. In

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middle ear is inherently superior in sensitivity or fidelity to that of crocodilians, birds, or most lizards. However, the inner ear of mammals is markedly more sensitive than that of reptiles (Manley, '72). Many living reptiles do not conform in middle ear configuration to that just described (Barry, '63). In some, such as the chameleons, the depressor mandibulae muscle covers the entire postquadrate region where a thin tympanic membrane would be expected (Olson, '66). Air-borne T h e middle ear of living reptiles sound is sensed fairly well by some chameBest known of reptilian ears is that leons, but by a surprising mechanism: the of "typical" lizards with a well-developed inferior temporal fenestra is the primary tympanic membrane and cavum tympani region of reception, the functional eardrum (figs. 2A,B,C). Here the eardrum is a thin being the thin pterygoid bone (contacted sheet, convex externally, which is supported by the columella) beneath a sheet of musby the high, mobile, deeply excavated cle (Wever, '68). Chameleons have a large quadrate. Drum vibrations are transmitted cavum tympani, but amphisbaenids have by a single skeletal element of hyoid arch neither cavum tympani nor tympanic memderivation. This, the columella or stapes, brane and possess a long extrastapes which consists of an ossified footplate-bearing passes along the lateral aspect of the manproximal portion (stapes proper) and a dible (and moves with it). Low-frequency cartilaginous distal portion (extrastapes or aerial sound is heard well, vibrations being extracolumella). The latter has a stem initiated in large scales overlying the and several processes: a small dorsal proc- mandible and transmitted by the extraess connecting by ligament to the carti- stapes (Gans and Wever, '72). Snakes also laginous intercalare between the quadrate lack cavum tympani and eardrum yet are and opisthotic; a slender quadrate (inter- sensitive to air-borne sound of low hz, nal) process connecting by ligament to the which is received by the general region of quadrate; a small hyoid (posterior) process the head and even by the body with transembryonically continuous with the anterior mission via the lung (Hartline, '71). Sphehyoid cornu; and the pars superior and nodon, in most respects the most primitive inferior of the tympanic extremity. Behind living reptile, retains throughout life an the eardrum passes the depressor mandib- attachment of the anterior hyoid cornu to ulae muscle which inserts on the posteriorly the extrastapes. Scaled skin covers an projecting retroarticular process of the aponeurotic "eardrum" behind the quadmandible. Essentially the same middle ear rate (Gregory, '51). Physiological studies construction is found in turtles (fig. 3 ) , on Sphenodon have not been reported. For crocodilians, and birds, with a cavum tym- further information on reptilian ears see pani and an externally convex eardrum Baird, '70). (overlain by horn plating in some turtles) Homologies supported by an excavated quadrate and To outline the full evidence for the hocontacted by a columella. All of these ears have a large drum-foot- mologies pertinent to this account is unplate ratio and, contrary to common opin- necessary in view of the extensive literature ion, a leverage mechanism (Manley, '72). on this subject (Gaupp, '13; Goodrich, '30); Leverage is provided in most lizards by the only a summary is presented. The mammalian jaw apparatus passes tympanic extremity of the extrastapes pivoting about its dorsal end, the force arm through a fetal stage strikingly similar in to the center of the drum (pars superior + morphology to adult advanced cynodonts pars inferior) exceeding the resistance arm (figs. 5, 6, 7A). At this stage, the malleus to the stapedial shaft (pars superior alone). may be considered part of the mandible While most mammals perceive consider- and the incus part of the suspensorium. ably higher sound frequencies than reptiles, The major portion of the malleus is, like there is no reason to think the mammalian the homologous articular of reptiles, the

most mammals i t later fuses to adjacent skull bones, but in some it remains loose (figs. 4A,B,C). In monotremes the large anterior process of the malleus is tightly bonded, often synostosed, to the loosely suspended tympanic anulus (fig. 4C) (Doran, 1879; Goodrich, '30). Malleus and tympanic probably vibrate as a unit in these mammals (Aitkin and Johnstone, '72), which 1 consider to be a retention of the primitive mammalian condition.

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ossified posterior end of Meckel's cartilage. The manubrium mallei corresponds to the ventrally projecting extension of the cynodont articular usually termed its retroarticular process. The main portion of the anterior process of the malleus develops from a separate, intramembranous ossification center generally considered the homolog of the reptilian prearticular (but see Olson, '44). The incus corresponds to the quadrate, its crus brevis and crus longus being homologous with the dorsal and stapedial processes, respectively, of the cynodont quadrate (fig. 6). Whereas malleus and incus are firstarch derivatives, the stapes is derived from the dorsal end of the second (hyoid) arch skeleton and is the homolog of the stapes proper and at least the proximal portion of the extrastapes of reptiles (including the quadrate process). The therapsid dorsal process has disappeared. According to Westoll ('44) the cartilages of Paauw and Spence found in some mammals are remnants of a former extrastapedial extension to the eardrum, but this is dubious in view of their late appearance ontogenetically (Schute, '56) and the absence of continuity between Spence's cartilage and the stapes in development. As first clearly demonstrated by Palmer ('13), the intramembranous tympanic bone is homologous with the reptilian angular, much of it corresponding to the cynodont reflected lamina (RL, fig. 6, 7A). Morphologically, the mammalian tympanic membrane and cavum tympani are farther anterior and ventral than in reptiles or birds (Shute, '56). Some embryologists (e.g. Gaupp, '13), but not others (e.g. Goodrich, '30), have considered these features to be independently evolved. The tensor tympani muscle which inserts on the malleus (TT, fig. 1) probably is a derivative of the posterior pterygoideus (sensu Barghusen, '73) of synapsid reptiles, as is the mammalian medial pterygoid muscle.

descent of mammals but nevertheless relevant to interpretation are also considered. Since soft tissues are rarely fossilized, only osteologic features can be directly documented. Reconstruction of soft tissues is largely deferred to later sections. Here, and elsewhere, I adhere to the taxonomic usage of Hopson and Kitching ('72) for the Cynodontia (thus tritylodonts and tritheledonts are considered advanced cynodonts) except that I treat the tritheledont marthrognathus as generically distinct from Pachygenelus; for all other groups I follow Romer ('66), except for the Bauriamorpha which I treat as advanced members of the Therocephalia. Reptiles are generally thought to have descended from labyrin thodont amphibians having an eardrum supported in a pronounced indentation (otic notch) in the rear margin of the skull, toward which a rather lightly built stapes projected (Hotton, '60; Olson, '71; Romer, '66; Watson, '51, '53). No otic notch is present in the earliest known reptiles (primitive captorhinomorphs and pelycosaurs), probably having closed up (Romer, '66, but see Panchen, '72). Also absent is any excavation of the quadrate as seen in living reptiles with tympanic membranes, and there is no conspicuous retroarticular process. If an eardrum was present there is no direct evidence of it. The stapes of captorhinomorphs and pelycosaurs, where known, is heavily built and projects toward a pit in the quadrate into which it probably continued in cartilage (Hotton, '60; Olson, '71 ; Romer, '56). Thus, in osteologic configuration the middle ear region of the earliest reptiles is not similar to that of typical living reptiles. Later captorhinomorphs developed a slight concavity of the posterior skull margin just above the jaw articulation, and a backward-jutting retroarticular process, changes suggestive of incipient auditory specialization of the sort seen in much more pronounced form in most modern reptiles and in birds. No such trends appeared osteologic evolution of the synapsid in synapsids, except for certain pelycosaurs middle ear and mandible unrelated to therapsid ancestry (Olson, '71). In this section a synoptic description is The rest of this section is organized by given of the major structural changes lead- structure: ing to the mammalian condition of mandible and middle ear, as revealed in the 1. The stapes fossil record. Organisms not on the path of In captorhinomorphs and pelycosaurs

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the massive stapes has a stout, proximally situated dorsal process articulating with the paroccipital process (posterolateral extension of the opisthotic bone). On the ventral side of the stapedial shaft in such pelycosaurs as Ophiacodon and Dimetrodon is a roughened depression thought to be the site of attachment of a strong ligament attaching the stapes to the anterior hyoid cornu (Romer and Price, '40). In Captorhinus there is some evidence for an attachment of the hyoid cornu to the distal end of the stapes posteriorly (Parrington, '46) as also appears to be true for a recently discovered specimen of the advanced captorhinomorph Labidosaurus with ossified hyoid cornua, as inferred from a photograph kindly provided by Prof. E. C. 01son. Thus, primitive reptiles probably had a persistent hyo-stapedial connection as does the living Sphenodon. Such a connection is present in the embryo in all amniotes. In a11 therapsid groups the stapes is considerably reduced in mass but retains an end-on contact with the quadrate, either in the form of a cartilaginous continuation into a pit (stapedial recess) in the quadrate (phthinosuchians, gorgonopsians, some therocephalians) or a direct bony abutment (anomodonts, advanced therocephalians, and cynodonts). A n ossified dorsal process, situated far distally, is present in at least some members of all groups (SD, fig. 20). In some dicynodonts there is reason to believe the primitive hyo-stapedial connection persisted (Barry, '68) but in other groups there is little evidence for such a connection; in certain advanced cynodonts there is good evidence that the anterior hyoid cornu attached to the tip of the paroccipital process instead, as in most living reptiles and mammals. Thus, Probelesodon and Probainognathus have at this point a pit or projection (HA, figs. 24, 25) surfaced in unfinished bone, as at the base of the cartilaginous styloid process of many mammals. 2. The suspensorium The quadrate of captorhinomorphs and pelycosaurs (figs. 16, 17) is high, massive, and virtually immobile (Romer, '56). Sutured to it laterally is the small quadratojugal which, in later sphenacodonts (i.e. sphenacodontids), is a slender vertical

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plate applied to the quadrate. Basal therapsids (phthinosuchians) are little changed from their sphenacodontid ancestors in any aspect of skull or jaw structure. The quadrate remains fixed in anomodonts (dinocephalians and dicynodonts) but has a simple, non-interlocking junction with the skull. In dinocephalians the quadrate remains large; in dicynodonts it is moderately reduced. The quadrate complex (quadrate and quadratojugal) is progressively reduced in mass in theriodont lineages by diminution of the dorsal portion of the quadrate. Advanced cynodonts also show reduction of the condylar portion of the quadrate associated with formation of an articulation between the surangular or dentary bone and the squamosal (Crompton, '72). Probably the complex was moderately mobile (streptostylic) in all theriodonts (Hopson, '69). In primitive theriodonts (gorgonopsians and early therocephalians) the rounded posterodorsal aspect of the quadrate complex nestles into a shallow depression in the squamosal (Kemp, '69; Parrington, '55). In advanced therocephalians (whaitsiids, scaloposaurs, and bauriamorphs) and in cynodonts there are separate, deep sockets in the squamosal for the dorsal portions of the quadrate and quadratojugal (figs. 23, 24, 25) (Crompton, '64, '72; Kemp, '72a,b). Extreme reduction of the quadrate and the strength of its moorings occurs in tritylodonts (fig. 8) and tritheledonts (fig. 9) (Crompton, '63, '64, "72). 3. T h e mandible Early captorhinomorphs and pelycosaurs are much alike in mandibular structure (fig. 17). Seven or eight elements, united by irregular sutures, compose each hemimandible. These are the tooth-bearing dentary and a series of "accessory" jaw elements: the articular, prearticular, angular, and surangular (these four I will refer to as the postdentary elements) as well as the splenial, coronoid, and anterior coronoid (lost in later reptiles). No marked coronoid eminence (elevation of the posterodorsal margin of the jaw) or retroarticular process is evident. A large adductor (levator) fossa for insertion of jaw musculature is present. In advanced captorhinomorphs, as in labyrinthodonts and non-

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synapsid reptiles generally, the mandible is transversely thick, and rounded along its entire ventral border. In most synapsids, including primitive pelycosaurs, the mandible is transversely narrower (Romer, ’56). All advanced pelycosaurs except the caseids have a pronounced deepening of the posterior portion of the mandible and an adductor fossa which does not extend into the ventral part of the jaw as it does in most non-synapsids. Instead, a solid, thin keel of the angular projects ventrally. The keel is simple in form in Ophiacodon (Romer and Price, ’40) and a similar keel is present in at least one primitive captorhinomorph (Protorothyris, Barghusen, ’72). In advanced sphenacodonts, however, the keel is incomplete posteriorly and offset laterally as the reflected lamina (RL, fig. 16). Followed posteriorly, the free border of the reflected lamina runs dorsally in a sinusoidal curve to reach the body of the angular high on its lateral aspect. A rim of variable distinctness continues back from this point along the dorsal limit of the angular body, then curves downward along the lateral aspect of the ventrally projecting retroarticular process (RP, fig. 16) (Janensch, ’52, gives this projection the more descriptive term “infraarticular process’’). The space separating the posterior margin of the reflected lamina from the lateral rim of the retroarticular process, bounded dorsally by the rim on the angular body, can be visualized as produced by excision of the posterior portion of the angular keel of a primitive sphenacodont (fig. 17); I will term this space the angular gap. Probably in life it was bridged by a sheet of tough connective tissue. Exposed by the gap, in lateral view, is part of the angular body bearing on its lateral face a shallow concavity which I will label the external fossa (EF, fig. 16). The external fossa is continuous with a depression on the anterolateral aspect of the retroarticular process and extends anteriorly onto a part of the angular body hidden in lateral view by the reflected lamina. Posterodorsally, the smooth medial face of the reflected lamina curves abruptly to become continuous with the external fossa. Thus, the posterior portion of the angular is “split” to form two plates: the reflected lamina laterally, and the posterior portion of the body of the angular medially. The latter can be termed

the medial lamina of the angular body. The space bounded medially by the entire external fossa, and laterally by the entire inner face of the reflected lamina and the hypothetical connective tissue sheet bridging the angular gap, I will call the angular cleft (essentially synonymous with the less precisely defined “angular notch” of many authors). The suite of features just described (reflected lamina, external fossa, angular cleft and gap, and ventrally projecting retroarticular process) is also found, in varying form, throughout the therapsids and will be termed the angular complex. Other characteristics of the sphenacodontid mandible include a pronounced coronoid eminence, conspicuous partly because the articular region is “downwarped,” and a large protuberance of the articular medial to the retroarticular process which Romer and Price (‘40) consider to have served for insertion of part of the pterygoideus musculature (PtP, fig. 16). An apparently homologous process, farther dorsal and less conspicuous, is present in more primitive pelycosaurs and in therapsids, and perhaps persists in mammals as the muscular process of the malleus on which the tensor tympani inserts. In anomodonts the angular cleft is considerably deepened and the angular gap extended. The reflected lamina is thick in dinocephalians but thin and sometimes corrugated in dicynodonts. In some members of both groups the sagittally deep angular cleft is narrow transversely and the external fossa largely hidden from view by the expansive reflected lamina (e.g. Ulemosaurus, Efremov, ’40; Dinodontosaurus, Cox, ’65). In some dicynodonts the angular gap expands considerably at the expense of the dorsal portion of the reflected lamina. The dentary is not enlarged noticeably relative to sphenacodonts, but in dicynodonts it has a less complex suture with the postdentary elements and there is encroachment of jaw musculature onto the dentary (Crompton and Hotton, ’67). Many dicynodonts have a perforation of the mandible between dentary and postdentary components. Gorgonopsians and primitive therocephalians display an increased height but reduced transverse width of the postdentary portion of the mandible, simplification of the interface between dentary and post-

EVOLUTION OF T H E MAMMALIAN MIDDLE EAR

dentary regions, considerable deepening of the angular cleft and, except in some gorgonopsians, elongation of the narrow angular gap. The reflected lamina is wide but thin, and characteristically corrugated in therocephalians (Crompton, '72), thicker and with a deep depression and strengthening rib on its lateral aspect in gorgonopsians (Barghusen, '68; Kemp, '69). Some gorgonopsians have a long retroarticular process curving downward and anteriorly (Parrington, '55; Kemp, '69). Both groups show moderate expansion in height of the dentary, with formation of a distinct coronoid process. The immediate ancestry of the cynodonts is uncertain. In basic structure, the quadrate complex and mandible of early cynodonts conform quite closely to the pattern seen in advanced therocephalians, one or other group of which may well have given rise to the cynodonts (Hopson and Crompton, '69; Kemp, '72b). The hypothetical ancestral stage depicted in figure 15 represents essentially the advanced therocephalian condition (Barghusen, '68; Crompton, '55; Kemp, '72a,b). Here, the postdentary elements form a unit clearly distinct from the rest of the jaw. Between the flat anterior projection of the surangular dorsally and a strut formed by the prearticular and angular ventrally is a separation which is exposed in lateral view as an aperture behind the dentary. The anterior extensions of the surangular, prearticular, and angular are clasped between the dentary laterally and the coronoid and splenial medially. The medial lamina of the angular is a high plate. The angular cleft is deep sagitally but narrow, and the angular gap is long but not wide. A broad, thin, COITUgated reflected lamina largely covers the external fossa. There was no insertion of levator musculature on the lateral aspect of the dentary (Barghusen, '68). Very primitive cynodonts (procynosuchids) display the beginnings of the great expansion of the posterior portion of the dentary which characterized later cynodonts (Crompton, '63; Barghusen, '68, '72). kvator musculature had begun to encroach on the outer face of the dentary, as indicated by a shallow fossa on the low coronoid process (fig. 14). Posterior to the dentary the main mass of the mandible is a high, narrow, composite plate largely

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covered on its lateral aspect by a very extensive external fossa. The full dorsal extent of the reflected lamina is not certain and may have been greater than shown in figure 14. By the galesaurid (thrinaxodontid) stage (fig. 13) a high coronoid process has evolved, as well as a fully developed masseteric fossa. This, together with the associated outbowing of the zygomatic arch, establishes that a mammal-like masseter muscle had made its appearance (Barghusen, '68, '72). There is some reduction in height and mass of the postdentary unit, a trend which continues in all later cynodonts, independently in several lineages. The angular gap is very wide, exposing almost the entire external fossa in lateral view. The reflected lamina is somewhat reduced in breadth. As revealed in a sectioned specimen, the medial aspect of the dentary is smooth and slightly concave where it articulates with the postdentary elements. In advanced cynodonts the dentary assumes an increasingly mammal-like form, with a large, often recurved coronoid process and, jutting out from its base, a pronounced posterior process corresponding to the mammalian condylar process (COP, figs. 6, 7, 8, 9, 12) as well as a distinct angular process (AP, same figures). The posterior process, extending as a buttress dorsolateral to the surangular, presumably received jaw musculature formerly inserting on the surangular. Part of the masseter muscle almost certainly inserted on the angular process, most likely with fibers running posteroventrally like the superficial masseter of mammals. At least in cynodonts with a very pronounced angular process (e.g. Diarthrognathus, fig. 9) part of the pterygoideus musculature, formerly inserting on postdentary structures, had probably shifted to this process as in mammals. In very late cynodonts the postdentary elements form a compact rod ensconced in a smooth-walled trough in the dentary (Tr, figs. 7B, 8, 9) which may have a prominent dorsal lip, the medial ridge (MR), to resist upward displacement of the postdentary unit. The articular, prearticular, and surangular fuse. All advanced cynodonts except tritylodonts and tritheledonts have a new articulation between the posterior end

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of the surangular (surangular bosse, SAB, figs. 7A, 13, 24) and the squamosal, dorsolateral to the articular-quadrate joint (Crompton, ’72), which in life must have reduced the compressive load borne by the quadrate. An independently evolved dentary-squamosal articulation is present in Diarthrognathus (Crompton, ’63, ’72), at least one tritylodont (Fourie, ’68), and incipiently in Probainognathus (fig. 24) (Barghusen and Hopson, ’70; Romer, ’70). Such a joint would have reduced the stresses taken by both the postdentary unit and quadrate. The cynodont reflected lamina and retre articular process are rarely preserved. When intact, the reflected lamina of later cynodonts is a slender splint (Gregory, ’51; Palmer, ’13; Watson, ’51) (RL, fig. 7A), while the retroarticular process is variable in prominence (sometimes quite large, as in fig. 7A) and has a lateral concavity which is part of the external fossa. The portion of the external fossa on the angular is much reduced in height in advanced cynodonts (EF, figs. 12, 21, 24) but the angular gap remains quite wide. The earliest accepted mammals for which information is available conform in jaw structure to the advanced cynodont pattern, but have a well developed dentarysquamosal joint (fig. 11). The postdentary elements, housed in a smooth trough in the dentary, continued to function as part of the mandible and the quadrate as part of the suspensorium. In this sense the earliest mammals did not yet possess a “mammalian middle ear.” The dentary has been described in some detail for two genera of Rhaetic mammals, one therian (Kuehneotherium, Kermack et al., ’68), the other not (Eozostrodon (Morganucodon), Crompton, ’63; Kermack and Mussett, ’58; Kermack et al., ’73; Parrington, ’71). Incomplete postdentary elements and quadrate have been described for the latter (Kermack et al., ’73).2 In a t least two independent lineages of later mammals (leading to monotremes and advanced therians) the postdentary elements came to be completely divorced from the mandible as components of a middle ear of fundamentally the same unique design (Crompton and Jenkins, ’73; Hopson, ’66). Probably this had already occurred in late Jurassic therians, to judge by the

structure of the dentary which no longer has any trace of a trough for postdentary structures (Krebs, ’71). From the foregoing outline it will be seen that several moreor-less correlated trends demand explanation if the origin of the mammalian middle ear is to be explained: reduction in mass of the stapes; reduction in mass and loosening of the quadrate complex and the postdentary component of the mandible; expansion of the dentary and transference onto it of jaw muscle insertions; formation of an accessory jaw articulation (surangular-squamosal, then dentary-squamosal); formation of the angular complex, followed by expansion of the angular cleft and gap relative to the size of the postdentary elements, and thinning and reduction in area (following an initial expansion) of the reflected lamina. Several of these trends occurred in parallel in more than one lineage, including formation of the definitive mammalian middle ear. End-on contact between quadrate and stapes seems to characterize the whole of synapsid history, and in middle ear osteology the synapsids never much resemble typical living reptiles or birds.

The enigma of the angular complex The reflected lamina, characteristic of advanced sphenacodonts and all therap sids, has no obvious analog in other vertebrates. It is always present in association with the less clearly unique external fossa and downturned retroarticular process. These three apparently related features, together with the angular cleft and gap, constitute the angular complex. To explain any component of the complex it is probably necessary to explain all. It is difficult to determine the functional significance of structures unknown in living organisms, and diverse suggestions have been put forward concerning the angular complex. The crucial questions are these: what was the role of the reflected lamina, when and how 2 Kermack et al. (’73) may have exaggerated the mass of the postdentary elements in their reconstruction. The isolated articular complex which they consider to be from a juvenile (fig. 33) seems more likely to be from a larger specimen, to judge by the size of the postdentary fragments and quadrate i n the most complete specimen (figs. 31, 32). Even if this is not the case, their claim that the relative size of the “reptilian” jaw articulation of Morganucodon is as large a s in Cynognathus i s not supported by their illustrations (fig. 371, especially if the surangular boss (their “retroarticular process”) i s included.

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did it come to support the tympanic membrane, and what occupied the angular cleft? Three candidates for occupancy of the cleft have been proposed: muscle, salivary gland, and an air-filled diverticulum of the cavum tympani or pharynx. In most living reptiles and in birds, pterygoideus musculature wraps around the lower border of the mandible to reach the lateral aspect of the angular (PtM, fig. 2B) which sometimes has a shallow depression rather similar to the synapsid external fossa (especially in certain birds). Were i t not for the existence of the reflected lamina and the blade-like lower border of the medial lamina of the 'angular in some therapsids, I might agree with Barghusen ('68, '72), and others who reconstruct therapsid pterygoideus musculature as inserting in, and filling, the external fossa (PtM, fig. 26B). This seems unlikely, however, in therapsids having a broad reflected lamina largely covering a sagittally expansive external fossa, especially when the intervening angular cleft is transversely narrow as in dinocephalians, many dicynodonts (e.g. Dinodontosaurus, Cox, '65),and most therocephalians (fig. 15). Muscle occupying such an enclosure would function very inefficiently, since it would be unable to shorten without bulging against its skeletal confines as well as constricting off its own blood supply, although an associated venous plexus might provide volumetric compensation. Muscles enclosed by bone do exist (e.g. stapedius in mammals) but are very uncommon. A tendon sheet might enter a narrow space, but the completely smooth surface of the external fossa in all therapsid specimens I have inspected or seen described argues against this, and there is no evident advantage in such a tendon sheet over attachment along the ventral margin of the jaw. In addition, it is unlikely that muscle or even tendon would wrap around the sharp ventral margin of the mandible in such therapsids as the gorgonopsian Arctognathus (Kemp, '69), various therocephalians, and some cynodonts (e.g. Massetognathus), although if muscle inserted on the medial aspect of the jaw down to the border, muscle fibers might circumnavigate a sharp edge without angulating sharply. In living reptiles and birds the ventral border of the jaw is usually smoothly rounded. These argu-

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ments favor the conclusion that at least in many therapsids the angular cleft was not filled with muscle. Pterygoideus musculature probably inserted extensively on the posteromedial aspect of the postdentary region, including the retroarticular process, and possibly in the depression on the anterolateral aspect of the retroarticular process. Romer and Price ('40) present a strong case for insertion of pterygoideus musculature on the medial aspect of the angular keel in non-sphenacodont pelycosaurs such as Ophiacodon, as well as on adjacent parts of the posteromedial region of the jaw. In their view, as the articular region descended in sphenacodonts, the angular keel shifted laterally to prevent restriction of the pterygoideus, and the angular gap developed to permit free expansion of this muscle during shortening. Thus, the pterygoideus musculature of advanced sphenacodonts filled at least part of the angular cleft, inserting on the medial face of the reflected lamina. Barghusen ('68, '72, '73) reconstructs this musculature similarly for advanced sphenacodonts, but with insertion extending into the external fossa and, if present on the reflected lamina, restricted to its posterior portion. He points out ('73, fig. 6) that one specimen of Dimetrodon (MCZ 1348) has distinct, low horizontal ridges in the dorsal part of the external fossa posterior to the reflected lamina, indicating muscular attachment. I agree with his interpretation for sphenacodontids, but not therapsids. Broom ('32) thought a salivary gland resided in the angular cleft. This is very unlikely. Salivary glands probably did not exist in sphenacodonts or primitive theriodonts, which did not masticate. Also, a gland would surely not have so special a skeletal accommodation as the angular complex; the mammalian parotid gland is similarly located but has no such housing. Following Palmer's ('13) demonstration of the kinship of the late cynodont angular and mammalian tympanic, it was believed by many morphologists that the tympanic membrane of therapsids and advanced sphenacodonts was situated in the angular gap, underlain by an &-filled chamber in the angular cleft (Parrington, '49; Sushkin, '27; Watson, '14). The concept of an eardrum in the angular gap eventually lost

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support for the reasons given below, but the concept of an air chamber in the angular cleft which served a non-auditory function (Westoll, '43, '45) continues to have adherents (fig. 26C). Westoll argued that most probably the chamber was a diverticulum of the cavum tympani (his recessus mandibularis), but possibly a direct outpocketing of the pharynx (whether he would use the term recessus mandibularis for this is unclear, but I will do so). In his opinion the recessus is most likely to have functioned initially as a vocal resonator; only after the postdentary elements and quadrate had become greatly reduced (for nonauditory reasons), probably beyond the cynodont grade, could they be set into effective vibration by air-borne sound. The outer wall of the recessus then became the pars tensa of the mammalian eardrum, the old reptilian postquadrate tympanic membrane becoming vestigial as the pars flaccida. Schute ('56) agreed with Westoll except that he considered it likely that the therapsid mandibular air chamber was a pharyngeal diverticulum corresponding to the lateral extension of the lacertilian pharynx, immediately subjacent to the pterygoideus muscle, which he named the sulcus pharyngis submandibularis (SPS, figs. 2A,B). He suggested that originally the recessus mandibularis may have served an accessory respiratory function (COzelimination), as does the lizard submandibular sulcus, eventually relinquishing this role to the improved lungs and becoming the mammalian middle ear chamber, either alone or by coalescing with an existing reptilian cavum tympani. A recessus mandibularis would have much the same topographic relationship to jaw structures as has the mammalian cavum tympani to homologous structures, and there is nothing in the anatomy of the angular complex of therapsids to rule out such a chamber. The pterygoideus musculature would provide a path, as it were, for extension of the diverticulum around the ventral side of the mandible into the external fossa of therapsids. On strictly morphological grounds the case for a recessus mandibularis is inconclusive, but if function and evolutionary trends are also considered the case becomes strong (see below).

To date, three possible functions for the reflected lamina (not mutually exclusive) have been proposed: maintaining patency of a recessus mandibularis (a suggestion implicit in the idea of such a chamber); providing support for a tympanic membrane in the angular gap; and providing attachment for muscles. The first of these possible functions is highly probable if a recessus mandibularis existed; the second is very improbable if the usual assumption is made that there was a direct stapedial contact with the eardrum, as in typical living reptiles. Romer and Price ('40) pointed out that to reach the angular gap would require an extrastapes of considerable length and tortuous course, which would move with the mandible so hearing would be impaired during use of the jaws. They also noted that an eardrum confined to the gap of sphenacodontids would seem too small for the massive stapes. A tympanic membrane in the long, curving, narrow angular gap of dinocephalians or advanced therocephalians (fig. 15) would make functional sense only if the extrastapes ran along almost its entire length. Equally unlikely is the suggestion that a portion of the eardrum in the angular gap was continuous across the lateral side of the retroarticular process with a postquadrate portion of the drum to which an extrastapes projected (Watson, '14, '51). Usually there is no discontinuity of the rim forming the retroarticular boundary of the gap, and even if there were, a narrow isthmus would exist between the anterior and posterior drum segments, so the former would be nonfunctional. Furthermore, the posterior drum attachment figured by Watson ('51, '53) for Diademodon (Gomphognathus) is in an unlikely location (see below). A n eardrum confined to the angular gap and not contacted by the stapes is plausible for cynodonts but not for most members of other groups because such a drum would be too small for the mass it would be required to set into vibration. Muscles suggested as having inserted on the reflected lamina include: (1) pterygoideus musculature inserting medially (sphenacodontids: Romer and Price, '40; gorgonopsians and whaitsiids: Kemp, '69; '72a). This is plausible for groups in which the reflected lamina would have been able

EVOLUTION OF THE MAMMALIAN MIDDLE EAR

to resist fairly strong medially directed forces (sphenacodontids, gorgonopsians, dinocephahans) but dubious for other groups, in which the lamina is thinner. Kemp's ('72a) argument that bulging of the contracting muscle would counteract medial displacement in whaitsiids could only apply to the dorsal part of the reflected lamina, which overlies the angular body, not for the large ventral part which extends well below it. (2) Superficial masseter inserting laterally (Parrington, '55; Crompton, '63, not '72). Barghusen ('68) has convincingly ruled this out. (3) A slip of adductor externus in gorgonopsians inserting on the lateral side of the lamina (Barghusen, '68; Kemp, '69). This suggestion may well be correct, but only applies to gorgonopsians. (4) One or more thin, sheetlike muscles pulling in a ventral or posteroventral direction: intermandibularis (Watson, '5 1, '53), branchiomandibularis (Barghusen, 'SS), or constrictor colli modified to act as a depressor (Janensch, '52). To this group I would add a muscle similar to the cervicomandibularis of lizards (DM2, fig. 2C) (Camp, '23; Lightoller, '39). One or more of these suggestions seems likely to be correct. However, comparable muscles exist in many living vertebrates without any structure resembling a reflected lamina; it is unlikely that such musculature can provide a complete explanation for the reflected lamina. In summary, pterygoideus musculature probably occupied the angular cleft of sphenacondontids but in all but the most primitive therapsids an air-filled chamber extended into the dorsal portion of the cleft, its patency maintained by the reflected lamina which also provided attachment for one or more thin muscles pulling ventrally or posteroventrally. A recessus mandibularis was probably present in sphenacondontids ventral to the pterygoideus muscle mass, perhaps reaching the lower portion of the reflected lamina. The functional significance of the angular complex is discussed by Camp ('48) and Janensch ('52) and receives further attention below. The cynodont middle ear The key to the origin of the mammalian middle ear lies in correct interpretation of the cynodont condition. In cynodonts, un-

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like living reptiles having tympanic membranes, the quadrate has no obvious site of eardrum attachment, the squamosal and paroccipital process extend far downward behind the quadrate, and the long axis of the low-set stapes is directed toward the ventral extremity of the quadrate. Nonetheless, most authors have believed that a tympanic membrane contacted by a cartilaginous extrastapes was present posterior to the quadrate. Support for this conclusion was provided by Gregory's suggestion in 1910 that the characteristic groove passing down the posterolateral aspect of the cynodont squamosal, which I will call the squamosal sulcus (SqS, figs. 21, 23, 24, 25, 26A), housed a long, curving, tubular external acoustic meatus which terminated at a tympanic membrane behind the jaw articulation. Gregory pointed to the similar course of the squamosal sulcus of cynodonts and the long meatus of monotremes and opossums. Watson ('1 1) accepted this interpretation of the sulcus but proposed a somewhat different (and much more likely) site of attachment of the eardrum, this being, in Diademodon, an anteroposteriorly running squamosal lip immediately external to the paroccipital process. A similar squamosal lip is present in many other cynodonts (SqL, figs. 23, 24, 25). Since these early accounts there has been virtually complete agreement that the squamosal sulcus held a long meatus (e.g. Crompton, '64, '72; Gregory, '51; Hopson, '66; Olson, '44, '71; Parrington, '46, '49, '67; Romer, '56; Watson, '51, '53; Westoll, '43). Parrington's ('46) discovery of a laterally projecting bony process of the stapes in a specimen of Scalenodon (originally named Trirachodon angustifrons) (fig. 18A) appeared to confirm the existence of an extrastapes in cynodonts, usually cartilaginous and not fossilized, which projected to a postquadrate eardrum. Parrington concluded that the cynodont middle ear, while aberrant in several regards, was of fundamentally the same design as in "typical" hving reptiles. Figure 19 depicts his interpretation of middle ear osteology in a generalized cynodont, with the distal end of the stapes making very limited contact with the quadrate anteriorly and having an extrastapes (tympanic process, to be

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more explicit) posteriorly which projected directly laterally to reach, in life, the center of a tympanic membrane moored to the squamosal lip just lateral to the paroccipital process. Such a low-set eardrum might explain the downward projecting retroarticular process. However, there are problems with this conception of the cynodont middle ear. For one thing, the tympanic membrane as restored by Parrington (‘67) is disturbingly small relative to the fenestra vestibuli. Since there is no evident leverage mechanism, the transformer ratio would be very low and middle ear sensitivity would be lower still because of the relatively heavy stapes. An eardrum attached to the squamosal lip in Probainognathus could not have been much larger than Parrington’s version since it would be limited posteriorly by the hyoid cornu attached to the paroccipital process (HA, figs. 24, 25). Also, all livingvertebrates with tympanic membranes which have been investigated physiologically are known to have some form of middle ear leverage device (Manley, ’72). Another problem is that there is no evident reason to expect any cynodont with a middle ear of this sort to give rise to a descendant with a mammalian middle ear. Hopson (‘66) attempted to show how and why such a transformation might have taken place. He reasoned that once the articular and quadrate had become greatly reduced and a dentary-squamosal jaw point established under the influence of selective pressures related to feeding, the postquadrate eardrum developed an attachment to the retroarticular process and was able to actuate it. Together, the articular and quadrate provided a lever system enhancing auditory sensitivity, and the extrastapes disappeared because it “short-circuited” the new lever system. The angular element came to serve as mooring for the drum only after the angular process of the dentary, and with it the reflected lamina, shifted posteriorly in early mammals. While Hopson’s argument is carefully reasoned, it seems improbable that the cynodont ear lacked a leverage mechanism, which would probably be readily evolved either by development of an extrastapedial lever arm against the drum or by tilting of the drum relative to the stapes (Watson, ’51:p. 139). Also, i t is difficult to see why

the tympanic membrane, having been medial to the retroarticular process in cynodonts according to Hopson, would develop an attachment to it. Jaw movements would then impair hearing, a serious disadvantage in early mammals, which masticated their food and probably fed frequently. If the cynodont middle ear was as visualized by Hopson, it seems to me that the postdentary elements and quadrate should eventually have disappeared, leaving the stapes attached to the drum as the sole sound-conducting element. Parrington’s limited stapes-quadrate contact also must be questioned. The stapes is rarely intact and in place in cynodont specimens, but in undistorted skulls the fenestra ovalis generally faces directly toward the quadrate which, when well preserved, usually has a broad facet for articulation with the stapes. Furthermore, several specimens are known in which the stapes has a broad abutment with the quadrate (e.g. the Thrinaxodon specimens in figs. 20B, 23). It might be argued that the distal end of the stapes was displaced anteriorly postmortem; this can not be so for the Exaeretodon specimen illustrated (figs. 21,22), in which stapes and quadrate are definitely in natural articulation and the entire width of the distal end of the broad stapes articulates with the quadrate. Probably a much broader contact of stapes and quadrate than construed by Parrington (fig. 19) was the rule in cynodonts. Furthermore, there can not have been an “extrastapes” in Exaeretodon similar to that of Scalenodon (fig. 18) because a tubercle of the quadrate (QT, fig. 22) is in the way. Also, there is no unfinished bone on the posterolateral aspect of the stapes to suggest that a cartilaginous extrastapes was present in life. I have examined a cast of the Scalenodon specimen illustrated (fig. 18A). The stapes does have a distal process as Parrington stated. However, this process must have projected well lateral to the junction of squamosal sulcus and paroccipital process (fig. 18B). Such an “extrastapes” can not have projected to the center of a drum attached at the terminus of the squamosal sulcus; it would penetrate the tympanic membrane! What is more, it would probably have been flush with the back of the quadrate. Probably i t is best considered an

EVOLUTION OF THE MAMMALIAN MIDDLE EAR

extension of the usual contact of stapes and quadrate. Conceivably it might represent the base of a long extrastapedial process passing around the jaw articulation to reach the lateral aspect of the mandible as in amphisbaenids (Gans and Wever, '72). No other cynodont is known to have had such a process. Bonaparte ('66) describes a specimen of Exaeretodon showing the same stapesquadrate articulation as in figure 22. He remarks that the quadrate tubercle to which I have referred "takes the place of an extrastapes" (my translation), apparently thinking that the postquadrate tympanic membrane attached to it, making no contact with the stapes. Under these conditions the quadrate would have to vibrate for sounds to be heard. Such an arrangement, if characteristic of all cynodonts (Bonaparte makes no such claim), would make the origin of the mammalian middle ear somewhat easier to understand. It is unlikely, though, that both quadrate and stapes could be actuated by a small eardrum. Also, direct contact of stapes and drum would surely evolve. Because the most plausible site of attachment of a postquadrate tympanic membrane (the squamosal lip) is generally more or less in line with the stapesquadrate junction, a tympanic process of the stapes, if it existed at all, would probably jut abruptly posteriorly from the distal end of the stapes. It would provide a leverage device and would help to stiffen the eardrum. A rather similar angulated tympanic extension of the stapes is found in certain frogs (Werner, '60). However, there is no definite evidence for an extrastapes which contacted a postquadrate eardrum in any cynodont. Living vertebrates in which the stapes makes an end-on contact with the quadrate (apodans, many urodeles, snakes, and certain lizards) do not possess a tympanic membrane (Olson, '66). One author (Tumarkin, '55) asserts that none was present in cynodonts. I do not agree, but I am not convinced that cynodonts had an eardrum behind the quadrate. The strongest evidence for a drum in this location is the squamosal sulcus terminating behind the quadrate. However, the squamosal sulcus of gomphodont cynodonts seems far too wide for a meatus (e.g.

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Exaeretodon, fig. 21). I know of no living mammals, with the partial exception of the Suina, that have a long squamosal sulcus housing the external auditory meatus; at most there is a short concavity, usually small, immediately dorsal to the terminal portion of the meatus. The closest parallel in living vertebrates is the pronounced sulcus passing down the posterolateral aspect of the squamosal in turtles (SqS, fig. 3), which terminates posterior to the jaw articulation and lateral to the paroccipital process, often in a low ridge resembling the cynodont squamosal lip (Gray, 1869). The squamosal sulcus of turtles does not house a meatus or end at a tympanic membrane (the eardrum being supported by the quadrate anterior to the sulcus). Instead, the depressor mandibulae muscle fills the sulcus. A rather similar but less conspicuous depression for the origin of this muscle is found in many birds. I am inclined to believe that the squamosal sulcus of cynodonts also was occupied by a depressor mandibulae muscle inserting, at least in part, on the retroarticular process (fig. 26E). This possibility, apparently favored by Camp ('48), was considered by Watson ('11) but rejected because no retroarticular process was then known in cynodonts. Janensch ('52) considered i t unlikely that a depressor muscle attached to the therapsid retroarticular process, but for reasons that are weak (see Gans, '66). It might be argued that the sulcus is too tortuous for a depressor muscle to follow (in Exaeretodon for example, in which it turns medially behind the quadrate). This would be true if the muscle fibers were oriented in parallel with the sulcus, but not if they radiated upward from the retroarticular process to attach along the sulcus. It might also be argued that the sulcus in gomphodonts is too large for a depressor muscle, but the sulcus in turtles is often large and the depressor mandibulae is quite massive in such reptiles as the gavials. Also, in gomphodonts it is possible that the muscle served as a mandibular retractor in addition to its depressor action. If such a muscle did occupy the cynodont squamosal sulcus, there would not have been room for a meatus to reach a postquadrate eardrum and probably no such drum was present. In dinocephalians

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a long depression runs vertically down the ponent of the tympanum, not simply part posterior aspect of the squamosal. This of its mooring, an important distinction in seems to correspond to the sulcus of cyno- the case of primitive cynodonts in which donts, and has generally been interpreted the reflected lamina constituted a signifias housing a long meatus (e.g. Watson, cant proportion of the total sound-recep'14). But in Struthiocephalus the sulcus tive area. Vibrations of this drum were does not terminate in proximity to the transmitted by the postdentary unit, quadstapes (Boonstra, '53); very probably i t rate compIex, and stapes.3 In advanced housed a depressor muscle in all dinoce- cynodonts the mode of vibration and leverage mechanism of the postdentary unit phalians. Expansion of the cynodont temporal and quadrate probably would have been fossa to permit posterior enlargement of approximately the same as for the homothe temporalis muscle was partly achieved logous malleo-tympanic unit and incus of by flaring of the nuchal crest posteriorly monotremes except that vibratory deformaand eversion of the dorsal crest of the pos- tion of the reflected lamina would have terior root of the zygomatic arch, along occurred. Only long after the postdentary with downswinging of the point of conflu- unit had departed from the mandible in ence of these crests to accommodate tem- primitive mammals could the angular (tymporalis fibers inserting on the recurving panic) element be stabilized as a static tip of the coronoid process. Formation of (non-vibrating) drum-supporting entity; the cynodont squamosal sulcus may have this never took place in monotremes. Plate been largely incidental to these modifica- 6 depicts the skull and mandible of Thrintions and quite possibly it had no special axodon (fig. 26A) and four different reconstructions of relevant soft parts. Figures contents or significance. From the nature of its junction with the 26B,C represent the interpretations curstapes, the cynodont quadrate obviously rently most in favor, while figures 26D,E took part in sound conduction, relaying represent interpretations I consider more mandibular vibrations. Substrate-carried probable. The cynodont dentary-postdentary intersound would have efficiently passed by this route when the jaw was in contact with face, a simple non-imbricated syndesmothe ground. Cynodonts were surely sensi- sis, would have permitted efficient vibrative to air-borne sound as well, since even tion of the postdentary unit with minimal snakes, with no tympanic membrane, per- loss of sound energy to the dentary. Simiceive low-frequency aerial sound quite larly, the small quadrate complex, attached acutely. If cynodonts spent less time lying to the skull by ligaments, was surely capaprone than typical reptiles, as seems likely, ble of efficient vibration with little loss of then selection would probably strongly fa- energy to the skull. Transmission from arvor enhancement of aerial hearing. But if ticular to quadrate and quadrate to stapes it is true that no postquadrate eardrum would have been effective. It is essential was present in cynodonts, how would this to transpose mentally from the hard, have been achieved? Knowing the eventual heavy, inflexible nature of fossils to the fate of the postdentary elements and quad- very different character of living tissues, rate in their mammalian descendants, the and to recognize that the vibratory movepossibility must be entertained that in cyno- ments would be at most one or two angdonts these structures were already in- stroms (hundred-millionths of a centimeter) volved in reception of air-borne sound. I in amplitude, assuming sensitivity equal to that of snakes for mandibular vibration believe this was indeed the case. As argued earlier, the angular cleft in (Hartline, '71). therapsids harbored a recessus mandibuBecause the mandibular drum of cynolaris. It is my contention that in all cyno- donts would have been very large in area donts the eardrum consisted of the tissues relative to the stapedial footplate (in a superficial to this chamber, i.e. the re3 If pterygoideus musculature occupied the external flected lamina and a tense soft-tissue sheet fossa and the recessus mandibularis did not extend spanning the angular gap and extending dorsal to the reflected lamina, the tissues overlying the and muscle, including the reflected lamina, ventrally to reach the anterior hyoid cornu. recessus may nonetheless have served as tympanum (though inThe reflected lamina was a functional com- efficiently).

EVOLUTION OF T H E MAMMALIAN MIDDLE EAR

ratio of at least 30 to 1) and the lever ratio of the cynodont middle ear substantial, the overall transformer ratio would probably have been high relative to modern mammalian middle ears (Webster, ’66). Furthermore, the mass of the vibrating structures relative to the drum would be little greater in advanced cynodonts than in monotremes. Thus, although ligamentous and muscular impedance would have been greater in cynodonts, it is likely that middle ear sensitivity in advanced cynodonts approached that of living mammals. Primitive cynodonts, with relatively greater total mass of vibrating entities (postdentary unit, quadrate complex, and stapes) and greater ligamentous and muscular impedance, would have had lower auditory sensitivity, especially for higher frequencies. Having absolutely greater mass of vibrating parts and greater drum size, compared to the middle ear of living mammals, the cynodont middle ear would have had a lower natural frequency, thus lower responsiveness to high frequencies and higher efficiency for low frequencies of sound. Similarly, the sensitivity range of individual cynodonts would have shifted toward lower frequencies during growth. If the postdentary unit took part in the reception of aerial sound in the manner described, a number of otherwise puzzling circumstances become more understandable. Most strikingly, the transformation from the cynodont to the present-day mammalian condition of middle ear and mandible ceases to be mysterious. Also intelligible is the end-on quadrato-stapedial abutment. Further, the dramatic changes in structure of the mandible and suspensorium in the course of cynodont (and precynodont) evolution, changes which took place independently in several lineages, can be seen to represent a combination of auditory and feeding adaptations. Thus, loosening and reduction in mass of the postdentary unit and quadrate, and shifting of jaw muscle insertion onto the dentary, enhanced auditory efficiency by diminishing impedance (using “efficiency” in two senses: the amount of tissue required for a given level of performance; and the performance for a given level of incident sound energy, i.e. sensitivity). Similarly, expansion of the angular gap at the expense of the reflected lamina re-

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duced mass and decreased resistance of the lamina to vibration. The paradox of a great enlargement of jaw musculature over ancestral forms (as shown by expansion of the temporal fossa and the appearance of a masseter) accompanying simplification and reduction of the dentary-postdentary interface (i.e. enhancement of mandibular forces in concert with weakening of the junction between tooth-bearing and jawjoint-bearing components) can be understood as reflecting a compromise between auditory and mechanical demands. Special structural adjustments permitted reduction of the postdentary unit and quadrate and loosening of their moorings while maintaining adequate strength of the feeding apparatus. Descent of the squamosal behind the quadrate complex provided bracing against posteriorly directed forces, and deepening of the sockets for the quadrate complex provided improved resistance to vertical forces. Reduction of the dorsal part of the quadrate complex, and perhaps its ligaments, was made possible by these features. Development of a posterior process and medial ridge of the dentary braced the postdentary unit, permitting reduction in its vertical dimension. Formation of a surangular-squamosal joint facilitated reduction in size of the quadrate complex, and the later development of a dentarysquamosal joint permitted further diminution and loosening of the postdentary unit and its eventual complete separation from the mandible. A rather special geometry of muscle and reaction forces may have minimized stresses on the postdentary unit and quadrate complex, facilitating their reduction. Relative shifting of jaw muscle insertions anteriorly would have increased bite force while reducing vertical reaction force at the jaw articulation (Hopson, ’66; Parrington, ’34, ’55). Also, formation of a masseter muscle probably helped counteract transverse forces, along with the elongated vertical brace formed by the transverse process of the pterygoid bone (fig. 24, unlabelled), against which the coronoid element rode (Kemp, ’72b). Crompton (’63) argued for a balancing of forces in the. sagittal plane so that the jaw articulation was subjected to low stresses, especially in very advanced cynodonts. Certainly the remarkably feeble jaw joint of Oligokyphus, (fig. 8), if no sec-

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ondary articulation was present (Crompton, ’64), could not have resisted heavy stresses and must have been stabilized by the massive jaw musculature. However, in most cynodonts considerable reaction forces must have been absorbed at the jaw joint at times. It is generally thought that expansion of the dentary and the concomitant diminution and modification of postdentary elements, quadrate, and jaw articulation all occurred for mechanical reasons unrelated to hearing, and that direct involvement of postdentary elements and quadrate in aerial sound reception commenced subsequent to (or shortly before) establishment of the dentary-squamosal joint. Authors expressing this viewpoint include Broom (’12, ’32), DuBrul (’64), Hopson (‘66), Manley (’72), and Watson (’53). Another is Schute (’56: p. 276), who remarks that a tympanic membrane supported by the angular of advanced cynodonts “could have had little or no auditory function.” Crompton (’72: p. 231) states “it is generally accepted that formation of a dentary-squamosal joint “allowed the reduced quadrate and articular to assume a sound-conducting role.” Davis (’61: p. 231) claims “we may confidently assume that the compound reptilian mandible was replaced by a single pair of dentary bones because the compound construction was far less capable of withstanding the forces developed during mastication.” Kemp (‘72b) presents quantitative information to demonstrate that a compound mandible would be strengthened by eliminating sutures (syndesomes). He asserts that expansion of the dentary had this effect and remarks that “boundary weakness” at the simplified dentary-postdentary interface was not a problem since the rest of the mandible had sufficient strength. He does not attempt to explain the boundary weakness, but Kermack et al. (’73) argue that imbrication disappeared because it was rendered unnecessary by the strengthening effect of dentary expansion. If mandibular strength was at a premium it seems contradictory that weakening should occur at the dentary-postdentary interface. So long as the dentition and jaw articulation were on separate mandibular components united by a plane of relative weakness, I doubt that expansion of the dentary would have strengthened the cyno-

dont jaw. If it did, it is surprising that this has not occurred to anything like a comparable degree in any other vertebrate group. Also, synostosis is a simpler mechanism for arriving at a stronger and more rigid mandible. All jaw elements are fused in birds and in some turtles. The reason given by Kermack et al. (’72: p. 160) for the same not occurring in theriodonts depends on inapplicable occlusal relationships. Evolution of mammal-like massetericotemporalis musculature would have necessitated formation of a high coronoid process and broad masseteric fossa (Barghusen and Hopson, ’70), but not necessarily exclusively provided by the dentary. In my opinion, dentary dominance in cynodonts, while influenced by multiple selective pressures, was to an important extent a reflection of auditory adaptation. Several authors have surmised that the postdentary elements of cynodonts may have taken part in hearing air-borne sound, but have been vague as to mechanism, hesitant, or inclined toward the view that such an auditory role was only incipient in advanced cynodonts (e.g. Crompton and Jenkins, ’73; Gregory, ’13, ’51; Kermack, ’72; Sushkin, ’27; Watson, ’51,’53; Westoll, ’45). No previous writer has explicitly implicated the reflected lamina as a soundreceiving structure or emphasized auditory adaptation as an important factor in evolution of the cynodont jaw. Most previous writers have believed, partly on theoretical grounds, that cynodonts had a postquadrate tympanic membrane and extrastapes. I am not prepared to dogmatically reject this possibility. If it is correct, then probably the mandibular component of the tympanic apparatus served for reception of lower sound frequencies, the postquadrate component for higher frequencies (analogous bimodal sensitivity is shown for fkogs by Lombard and Straughan, ’74), losing its usefulness as the mandibular ear decreased in size in early mammals. However, I would emphasize that it is unwise to assume that cynodonts, being reptiles, had a middle ear of the “typical” reptilian sort; many living reptiles do not have “typical” ears, yet perceive aerial sound by mechanisms seemingly less plausible than that which I have proposed for cynodonts.

The tympanic apparatus of other synapsids Although numerous investigators have

EVOLUTION OF THE MAMMALIAN MIDDLE EAR

expressed the opinion that some sort of postquadrate tympanic membrane was present in some or all pelycosaurs and noncynodont therapsids (e.g. Cox, '59; Devillers, '62; Hotton, '59, '60; Parrington, '45; Romer and Price, '40; Watson, '14, '51), the evidence is not strong. Most pelycosaurs have no conspicuous skeletal indication of a site of drum attachment; a few have a shallow excavation of the posterior skull margin (Olson, '71), which may have supported an eardrum but may equally well have related to neck and depressor mandibulae muscles, as does a rather similar skeletal conformation in crocodilians. The small posterior projection of the paroccipital process of some dicynodonts, considered by Cox ('59) to have supported an eardrum, also could have served for muscle attachment. The sulcus on the posterior aspect of the squamosal in dinocephalians, as mentioned, and gorgonopsians (Gregory, '51; Watson, '51) probably held a large depressor mandibulae muscle; if so, no postquadrate tympanic membrane can have been present. A stapedial process interpreted as an ossified extrastapes (tympanic process) has been reported for a small number of therapsid specimens, including a dicynodont and certain gorgonopsians and therocephalians (Broom, '36, '37; Olson, '44). It has since become clear that in most if not all cases these are in reality misinterpreted dorsal and quadrate (internal) processes (see Parrington, '45). A facet on the stapes of a dicynodont has been considered to be the site where a cartilaginous extrastapes emerged in life (Cox, '59). This is, of course, indirect evidence. Thus, no definite instance of a tympanic process of the stapes is known for any therapsid, and the same is true for pelycosaurs. Watson, in 1953, argued that the stapes of pelycosaurs was too massive and firmly articulated to have been actuated by a tympanic membrane of reasonable size and that none was present, these animals hearing only by bone conduction. Hotton ('59) asserted that the stapes cannot have been too firmly moored to vibrate (correctly, in my opinion) and attempted to show experimentally that a small drum could set a massive stapes into audible vibration (but Manley, '72, considers better calibration necessary to establish this). In my opinion, it is probable that no postquadrate tym-

419

panic membrane was present in sphenacodonts or non-cynodont therapsids, but that all of these reptiles were able to hear air-borne sound (see below). The therapsid group most informative as to the origin of the cynodont auditory mechanism is the Therocephalia. In advanced therocephalians the stapes appears to have met the quadrate in much the same end-on contact as in cynodonts (Broom, '12; Broom and Robinson, '48; Kemp, '72a), notwithstanding Brink's ('63) restoration of the stapes of Bauria projecting posterior to the quadrate (in his three specimens with the stapes in situ it was directed squarely at the quadrate). Also, the postdentary portion of the mandible is lightly built, with a large expanse of thin subcutaneous bone including the reflected lamina (especially in lctidodraco, Broom and Robinson, '48), and with a deep angular cleft, an elongate angular gap, and a simple, planar dentary-postdentary interface (Kemp, '72a). The aperture through the mandible behind the dentary (fig. 15) probably had no special contents, being an area of low stress where bone was not required (Kemp, '72a). It contributed to minimizing postdentary mass, as did extension of the angular gap and thinning of the reflected lamina (corrugated to maintain adequate strength). These observations, together with the lightness and looseness of the quadrate complex, indicate clearly that the advanced therocephalian tympanic apparatus was much the same as in cynodonts, but with the reflected lamina making up a larger proportion of the soundreceptive surface. The same appears to be true for primitive therocephalians, such as pristerognathids, but auditory efficiency would have been considerably less owing to greater mass of the vibrating parts. In other therapsids and in sphenacodonts evidence for participation of jaw elements in the reception of air-borne sound is less clear. There is no conspicuous specialization for this function in sphenacodonts or phthinosuchians. It is questionable whether the heavy refiected lamina of dinocephalians could have been set into audible vibration except by very loud sounds. In most gorgonopsians the reflected lamina also seems rather ill-suited for sound reception, but the dicynodont angular complex seems well suited for this function. Both gorgonopsians and dicynodonts show certain

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features suggestive of significant involvement of jaw structures in aerial hearing: diminution of the quadrate complex (and loosening in gorgonopsians), some simplification of the dentary-postdentary interface, and increased attachment of musculature to the dentary. The aperture between dentary and postdentary jaw components in many dicynodonts probably had the same significance as in therocephalians; other than this, there is no obvious reduction of the postdentary portion of the jaw in anomodonts or gorgonopsians.

Synopsis of amniote middle ear evolution A tentative outline of the events leading to the typical reptilian middle ear on the one hand and the mammalian middle ear on the other can now be attempted, without development of the supporting evidence for certain conclusions not discussed above. In the earliest reptiles (basal captorhinomorphs) the ancestral labyrinthodont otic notch closed and both the tympanum i t had supported and the primary stapedial tympanic process were lost. The middle ear chamber persisted, extending posteriorly deep to the sheet-like primitive depressor mandibulae muscle and the dorsal extremity of the anterior hyoid cornu. Substrate vibrations reached the stapes via the anterior hyoid cornu and via the mandible and quadrate. Aerial sound waves set up vibrations in the thin tissues, including muscle, overlying the cavum tympani posterior to the skull, these vibrations reaching the stapes by way of the hyoid cornu. Refinement of this primitive apparatus led to the typical reptilian and avian middle ear, with a more efficient, musclefree drum (true tympanic membrane), loss or diminution of the hyo-stapedial connection, and modification of the stapes for improved aerial hearing. Primitive pelycosaurs developed either a ventral extension of the cavum tympani or an enlarged sulcus pharyngis submandibularis. The recessus mandibularis so formed served in part as an accessory respiratory device, but also took part in aerial sound reception, the overlying throat tissues serving as tympanum and vibrations passing via the hyoid cornu to the stapes. An additional mechanism of transmission, probably less important in early forms, was via the mandible and quadrate, with the

exposed posterior portion of the mandible also serving as tympanum. The postquadrate region lost its primitive tympanic function, perhaps because of enlargement of the depressor mandibulae muscle. Whatever the reason, a basic dichotomy in auditory strategy developed almost at the base of the reptilian stock. The reflected lamina of sphenacodontids and the angular keel of other pelycosaurs served, in part, to maintain tension in the superficial throat tissues and to hold open the recessus mandibularis, but the angular cleft of sphenacodontids was largely filled with pterygoideus muscle. In therapsids the angular cleft deepened to permit expansion of the recessus mandibularis dorsal to the pterygoideus insertion. The reflected lamina initially served primarily to hold open the recessus. Thinning of the reflected lamina and expansion of the angular gap at the expense of the reflected lamina reduced unnecessary bulk. The angular gap was bridged by a strong membrane. An initially incidental but, in some lines, eventually dominant factor in these changes was auditory improvement. In therocephalians, cynodonts, and dicynodonts, the mandibular tympanum became the main device for aerial sound reception. The hyoid-stapes transmission route decreased in importance, and was eventually eliminated, at least in cynodonts. Refinement of the cynodont middle ear, without fundamental change in mechanism led to the present-day mammalian middle ear. CONCLUDING REMARKS

My main conclusions are that in all cynodonts and therocephalians the postdentary portion of the mandible played a major role in reception of air-borne sound, the reflected lamina serving as part of the sound-receptive surface; that in these forms auditory adaptation was an important factor in the evolution of the mandible and suspensorium; and that the middle ear of living mammals (especially monotremes) continues to function essentially as in their cynodont predecessors. These conclusions are, I believe, consistent with all existing established data4 and have considerable explanatory power. See footnote 4 on page 421.

EVOLUTION OF THE MAMMALIAN MIDDLE EAR

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Broom, R., and J. T. Robinson 1948 On some new types of small carnivorous mammal-like reptiles. In: Spec. Public Roy. SOC.South Africa, For access to materials and facilities, I Robert Broom Commemorative Volume, pp. thank Professors H. R. Barghusen, A. W. 2944. Crompton, J. A. Hopson, N. Hotton 111, and Camp, C. L. 1923 Classification of the lizards. the late Prof. A. S. Romer. For valuable Bull. Am. Mus. Nat. Hist., 48: 28%481. 1948 The dicynodont ear. Spec. Public. discussions, I am grateful to all of them -. Roy. S O ~South . Africa, Robert Broom Commemand to Prof. J. W. Osborne. I am especially orative Volume, pp. 109-1 11. indebted to Prof. Barghusen for critical Cox, C. B. 1959 On the anatomy of a new dicyadvice on the manuscript. This work was nodont genus with evidence on the position of supported by a General Research Support the tympanum. Roc. Zool. SOC.(London), 132: 321-367. 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Abbreviations A, Articular bone AF, Adductor (levator) fossa AM, Adductor (levator) mandibulae externus muscle An, Angular bone AnA, Anterior process of angular bone AnB, Body of angular bone AnK, Keel of angular bone AP, Angular process of dentary API, Incipient angular process of dentary AT, Auditory tube C, Coronoid bone CA, Anterior coronoid bone CB, Crus brevis of incus CL, Crus longus of incus Co, Condyle of dentary CoI, Incipient condyle of dentary COP, Condylar (posterior) process of dentary CP, Coronoid process of dentary CS, Site of attachment of coronoid bone CT, Cavum tympani D, Dentary bone DA, Anterior belly of digastric muscle DM, Depressor mandibulae muscle DMl, Depressor mandibulae muscle proper DM2, Cervicomandibularis muscle DP, Posterior belly of digastric muscle E, Epitympanic recess of cavum tympani EAM, External acoustic meatus EF, External fossa EPt, External pterygoideus muscle ES, Extrastapes (tympanic process) FM, Foramen magnum FO, Fenestra ovalis (vestibuli) G, Glenoid fossa H, Anterior hyoid cornu sensu Zato (including mammalian styloid process and stylohyal ligament) HA, Probable site of attachment of anterior h jraid cornu HB, Hyoid body HP, Posterior hyoid cornu I, Incus IM, Intermandibularis muscle In, Intercalare J, Jugalbone JF, Jugular fossa LA, Anterior ligament of malleus LI, Posterior ligament of incus LS, Sphenomandibular ligament M, Malleus MA, Anterior process of malleus MC, Meckel's cartilage MF, Mandibular foramen MG, Groove for Meckel's cartilage

MM, Manubrium of malleus MR, Medial ridge of dentary My, Mylohyoideus muscle NC, Nuchal crest NQ, Notch i n squamosal for dorsal process of quadrate NQJ, Notch i n squamosal for quadratojugal P, Periotic bone PA, Prearticular bone PDR, Postdentary rod of fused elements PI, Pars inferior of extrastapedial tympanic extremity Po, Posterior (hyoid) process of extrastapes PP, Paroccipital process of opisthotic (or periotic) PS, Pars superior of extrastapes Pt, Pterygoid bone PtM, Pterygoideus muscle PtP, Process for insertion of part of pterygoideus musculature Q, Quadrate bone QCo, Condyle of quadrate QJ, Quadratojugal bone QSq, Depression in squamosal for quadrate QT, Tubercle of quadrate RC, Rectus cervicis complex (ventral longitudinal neck musculature) RL, Reflected lamina of angular RLB, Broken base of reflected lamina RM, Recessus mandibularis RP, Retroarticular process of articular RPB, Broken base of retroarticular process S, Stapes SA, Surangular bone SAB, Surangular boss for articulation with squamosal SC, Sphincter colli muscle SD, Dorsal process of stapes SH, Stylohyoideus muscle Sp, Splenial bone SPS, Sulcus pharyngis submandibularis SQ, Quadrate (internal) process of extrastapes Sq, Squamosal bone SqL, Squamosal lip sqs, squamosal sulcus SS, Sphenoid spine St, Stapedius muscle Sty, Styloideus muscle T, Tympanic membrane Tr, Trough in dentary for postdentary elements TrD and TrV, Dorsal and ventral parts of trough TT, Tendon of tensor tympani muscle Ty, Tympanic (ectotympanic) bone U, Unossified (cartilaginous) end of paroccipital process

PLATES

PLATE 1 EXPLANATION O F FIGURES

Except for figure 3, all figures on this and succeeding plates are original or redrawn from sources by the author, sometimes reversed for ease of comparison. A semidiagrammatic representation of the middle ear, mandible, and associated structures of a present-day mammal (neonatal higher primate) in medial view. Portions of the skull are removed to expose the middle ear cavity and the three ossicles: malleus (M), incus (I), a n d Stapes (S). The anterior ligament of the malleus (LA) a n d the sphenomandibular ligament (LS) a r e derivatives of Meckel's cartilage and its wrappimgs, as is t h e malleus. Fixed to the skull is the tympanic (ectotympanic) anulus (Ty) which supports the eardrum (T). The ossicular leverage system is indicated in heavy straight lines, the axis of vibration horizontal, the force arm and the shorter resistance arm vertical. A generalized lizard (based o n several sources and on dissection of Tupintimbis

te g n i x in ). Posterior view. The columella, situated well above the level of the j a w articulation, consists of a n ossified stapes proper (S) and a cartilaginous extrastapes (stippled) which contacts the tympanic membrane (T). The pharynx extends laterally beneath the pterygoideus muscle mass (PtM) as the sulcus pharyngis submandibularis of Schute (SPS). Lateral view showing the cavum tympani (CT), pharynx with sulcus pharyngis submandibularis (SPS), pterygoideus musculature (shown as transparent), a n d hyoid apparatus. The eardrum (T) is supported by the high, posteriorly concave quadrate bone (Q). Below i t the retroarticular process (RP) projects posteriorly. Lateral view showing superficial musculature. The depressor mandibulae muscle (DM1) passes behind the tympanum to insert o n the retroarticular process. The sheet-like cervicomandibularis muscle (DM2) (sometimes considered a portion of the depressor mandibulae) arises from the epaxial neck fascia a n d becomes aponeurotic superficial to the intermandibularis muscle (IM). Skull of the turtle Trtrchemys holbrookii, right lateral aspect (from Gray, 1869). A pronounced sulcus i n the squamosal (SqS) for the depressor mandibulae muscle r u n s vertically posterior to the quadrate (Q). T h e stapes proper (S) emerges through a notch in the deeply excavated quadrate which almost surrounds the tympanic membrane in life.

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EVOLUTION OF T H E MAMMALIAN MIDDLE EAK

PLATE 1

Edgar F. Allin

427

PLATE 2 EXPLANATION

4

428

OF FIGURES

Middle ear ossicles of primitive present-day mammals.

4A,B

American opossum ( D i d e l p h y s mcirszipztilisj, medial a n d lateral views. The stapes ( S ) is shown in dorsal view. The malleus (M) h a s a very large anterior process (MA) intimately attached (synostosed in this specimen) to the tympanic anulus (Ty),which is bonded to the skull only by loose connective tissue.

4c

Echnidna (Tcichyglosszts crcttletitus) (after Hopson, '66). The large anterior process of the malleus (MA) i s firmly attached, often by synostosis, to the loosely suspended tympanic bone (Ty). Probably malleus and tympanic covibrate in sound reception.

5

Ear ossicles a n d mandible of a fetal marsupial (Penrmelrs) in medial (5A) a n d lateral (5B) views (after Palmer, '13). Cartilage stippled. The malleus (M) i s the posterior end of Meckel's cartilage (MC). The incus (I) a n d stapes (S) are separate first- a n d second-arch derivatives, respectively. Three intramembranous bones are present: the dentary (D), a center for the anterior process of the malleus (MA), a n d the tympanic (Ty) which closely resembles the homologous angular element of advanced cynodonts (cf. fig. 7A).

6

An advanced cynodont possibly ancestral to mammals, Probtiirtog ntithzts j e n s e n i : mandible etc. i n medial view (right) (partly after Romer, '70) and quadrate complex i n posterior view (upper left, enlarged). The reflected lamina (RL) is largely hypothetical a s restored, being incomplete i n all available specimens. In this animal a surangular-squamosal a n d a n incipient dentary-squamosal articulation are present in addition t o the articular-quadrate joint. The quadrate is homologous with the incus, its dorsal and stapedial processes (QP a n d QS) corresponding to crus brevis a n d crus longus, respectively. The retroarticular process (RP) is the homolog of the manubrium mallei.

7

Mandible of Ditrdrmodon, a moderately advanced cynodont, in medial view with the postdentary elements (articular, prearticular, angular a n d surangular) i n place (7A) and removed (7B). The reflected lamina (RL) is restored after Palmer, ('13). The postdentary elements constitute a unit distinct from the rest of the jaw, lying in a smooth-walled trough in the dentary ( Tr D and TrV, fig. 7B). (After Crompton, '63.)

8

Mandible a n d quadrate of the advanced cynodont Oligokyphits, a tritylodont, i n medial aspect (after Crompton, '63, '64). Most of the retroarticular process is missing, a s is the anterior portion of the diminutive postdentary unit, revealing much of the smooth-walled trough in the dentary for its accommodation (Tr).

9

Mandible and quadrate of the advanced cynodont Diorthrog?ztrthrts, a tritheledont (after Crompton, '63, with the retroarticular process restored after Crompton, '72). As i n Oligolzyphiis a n d the earliest mammals the small postdentary unit (much of which is missing here) lies in a smooth trough (Tr) in the dentary. A pronounced medial ridge of the dentary (MR) overlies the trough. The feeble articular-quadrate j a w joint is supplemented by a dentary-squamosal articulation.

EVOLUTION OF T H E MAMMALIAN MIDDLE EAR Edgar F. Allin

PLATE 2

&€?

M

MA

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PLATE 3 EXPLANATION

OF FIGURES

A series of figures depicting structural modifications leading to the mammalian condition from a primitive sphenacodont ancestor. Two of the figures (15,17) are hypothetical; the rest are based on actual specimens which, while not necessarily in true a n cestor-descendant relationship, represent structural grades. For clarity, unknown or undescribed structures and details are reconstructed i n some instances. Left and right drawings are medial and lateral views, respectively. All are brought to uniform length although actual sizes are not uniform.

10

An early mammal in which the postdentary elements and quadrate are fully divorced from the mandible as tympanic (Ty), malleus (M), and incus (I). (Mandible of Amphitheriztm, after Hopson, '66 and pers. comm.; middle ear structures hypothetical and probably too reduced for this middle Jurassic pantothere.)

11

A Rhaetic mammal in which the postdentary elements and quadrate retain a suspensory function but a well developed dentary-squamosal articulation is present. (Based on Eozostrodon (Morgtrnztcodon), partly after Kermack et al., '73. Semidiagrammatic. Retroarticular process (RP) and reflected lamina (RL) hypothetical.)

12

An advanced cynodont with an incipient dentary-squamosal articulation (Probnino-

gntrthus, after Romer, '70, with reflected lamina (RL) restored). 13

A moderately primitive cynodont, Thrintixodon (after Crompton, '63; Fourie, '64).

14

A primitive cynodont (based o n Lecrvcichici, after Crompton, '63, '72,with reconstruction of the medial aspect and buried structures).

15 Hypothetical advanced therocephalian ancestral to cynodonts (based partly on Crompton, '55, and Kemp, '72a). 16

An advanced sphenacodont, Dimetrodon (after Romer and Price, '40, with approximate reconstruction of buried structures based on their sections).

17

Hypothetical ancestral sphenacodont in which the angular complex is not yet formed.

Stippled, Meckel's cartilage. Dotted line, hidden outline of surangular bone.

430

Dashed line, hidden outline of angular bone. Dot-and-dashed line, hidden outline of prearticular bone.

EVOLUTION OF THE MAMMALIAN MIDDLE EAR Edgar F. Allin

PLATE 3

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PLATE 4 EXPLANATION

18

O F FIGURES

A fragment of the skull of the cynodont Sctilenodon in ventral view with the stapes displaced (18A) (after Parrington, ’46). The quadrate is missing from its socket in the squamosal (QSq). Parrington interpreted the process at the distal end of the stapes as a n ossified extrastapes which projected to the center of a tympanic membrane at the termination of the squamosal sulcus (SqS), immediately lateral to the paroccipital process (PP). However, when the stapes is redrawn as if rotated and in approximately natural position (18B) the “extrastapes” projects well beyond the presumed site of eardrum attachment.

19 Parrington’s (’49) conception of the osteologic configuration of a generalized cynodont. Posteroventral view of the rear portion of the skull, left side. The stapes is depicted as having a dorsal process directed toward the paroccipital process of the opisthotic (PP) and a short, laterally directed extrastapes posterior to the medial end of the quadrate (Q).The stapes has only a very limited contact with the quadrate. The arrow passing along the sulcus in the squamosal (Sq) represents the assumed path of a long external acoustic meatus. 20

Stapes of Thriiurxodon (after Estes, ’61).

A

Left stapes in ventral, medial, lateral, and posterior views (upper left, upper right, lower left, lower right, respectively). The last is a silhouette of the anterior view given by Estes.

B

Right stapes (S), reversed to appear as left, showing a broad contact with the quadrate (Q). No extrastapes is evident.

21

Stereophotograph of the skull and mandible of the cynodont Extreretodov frenguellii MCZ 335-58M, ventral aspect, left side. A very large squamosal sulcus (SqS) is present, terminating posterior to the quadrate (Q). The stapes (S) has a broad articulation with the quadrate. The retroarticular process (RP) is conspicuous but only the broken base of the reflected lamina (RLB) is seen. The body of the angular element (fractured across) bears a smooth external fossa (EF). A prominent angular process of the dentary (AP) juts posteriorly ventral to the angular bone. The postdentary elements are displaced medially, revealing part of the trough in the dentary (Tr) for their reception (not completely cleared of matrix).

22

Stereophotograph at higher magnification of the broad junction of quadrate and stapes i n the same specimen as i n figure 21.The wellossified stapes shows no sign of an extrastapes of bone or a n unfinished site where a cartilaginous extrastapes might have emerged. Compare with figure 19.

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EVOLUTION OF T H E MAMMALIAN MIDDLE EAR E d g a r F. Allin

18 A

PLATE 4

20 A

B

23

PLATE 5 EXPLANATION O F FIGURES

23

Stereophotograph of a skull of T h r i n ~ i x o d o n liorhmus. Posteroventral aspect, right side. This beautifully preserved specimen shows clearly the articulation of the quadrate (Q) and quadratojugal (QJ) with the squamosal, and stapes (S) with the quadrate. The distal end of the stapes a n d of the paroccipital process (PP) are incompletely ossified. T h e shallow squamosal sulcus (SqS) terminates at a distinct squamosal lip (SqL).

24

Stereophotograph of the skull a n d mandible of Probtri,iogncith~isjr~srniMCZ 3801, ventral view, right side. The stapes is missing. The quadrate (Q) is very small and synostosed to the quadratojugal (QJ). The squamosal bears a glenoid fossa ( G ) for articulation with the surangular boss (SAB) and the incipient condyle of the dentary (displaced dorsally beyond view). On the angular body is a low external fossa (EF). Only the broken bases of the retroarticular process (RPB) and reflected lamina RLB) are present, as is usual in cynodont specimens. At the distal end of the paroccipital process (PP) is a raised area (HA) with a n unfinished surface, which probably represents the base of a cartilaginous styloid process (i.e. the site of attachment of the anterior hyoid cornu to the skull).

25

Stereophotograph of the skull of Probtrlnogncithzrs j r n s r n i MCZ 4017, i n lateral view (reversed). Quadrate and quadratojugal are missing from their smooth-walled sockets in the squamosal (NQ a n d NQJ). The squamosal glenoid fossa is hidden from view (dashed line). A pronounced projection ( H A ) from the distal end of the paroccipital process probably represents the base of a styloid process. If a tympanic membrane was attached to the squamosal lip (SqL), it must have been very small.

434

24

EVOLUTION OF T H E MAMMALIAN MSDDLE EAR E d g a r F. Allin

PLATE 5

435

PLATE 6 E X P L A N A T I O N OF FIGURES

Thrimtxodon, an early cynodont: skull and four reconstructions of soft-tissue structures. Skull (after Estes, '61, and Hopson, '66). The shallow squamosal sulcus (SqS) passes downward to end posterior to the quadrate (Q) (fig. 23). On its outer face the medial lamina of the angular body (AnB) bears the main portion of the smooth external fossa. The reflected lamina (RL) is thin and moderately broad. In this reconstruction the stapes (S) has a small contact with the quadrate (dotted outline) and a short extrastapes (ES) projecting laterally to reach the center of a small postquadrate tympanic membrane (T). The arrow indicates the course of a long, tubular external acoustic meatus passing along the squamosal sulcus. The anterior hyoid cornu ( H ) i s depicted as attaching to the paroccipital process and supporting the eardrum posteriorly. Filling the angular cleft is pterygoideus musculature (PtM). (Middle ear based on Hopson, '66, and Parrington, '49, '67; pterygoideus musculature after Barghusen, '68, '72). Here the stapes, tympanic membrane, and meatus (EAM, shown as a transparent tube) are the same a s in figure 26B, but the angular cleft is occupied by an airfilled chamber, the recessus mandibularis (RM), which is either a diverticulum of the cavum tympani or of the pharynx (i.e. a n enlarged sulcus pharyngis submandibularis). The recessus mandibularis does not serve a n auditory function. (Based on Westoll, '43, '45.) Here a postquadrate tympanic membrane is present, reached by a long meatus (arrow), a s in figures 26B,C. However, the stapes (dotted outline) h a s a broader contact with the quadrate and a slender extrastapes projecting posteriorly rather than laterally. A depressor mandibulae muscle (DM) passes around the meatus to reach the retroarticular process. A recessus mandibularis fills the angular cleft. The thin, tense tissues overlying the recessus mandibularis, including the reflected lamina, act a s a tympanum. Vibrations are transmitted from postdentary unit to quadrate to stapes. The reconstruction I consider most probable. There i s no postquadrate eardrum, extrastapes, or long meatus. The squamosal sulcus is occupied by the depressor mandibulae muscle. A s in figure 26D a recessus mandibularis is present, the overlying tissues serving a s tympanum. ( I t is possible, though improbable, that pterygoideus musculature occupied the external fossa a n d the recessus mandibularis did not extend dorsal to the reflected lamina; in that case, the tissues overlying the recessus, including the reflected lamina, may nonetheless have served as tympanum.) The tympanum would be quite strong, perhaps stiffened by keratin.

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EVOLUTION OF T H E MAMMALIAN MIDDLE EAR Edgar F. Allin

PLATE 6

437