Evolution of the Mammalian

A. W. Crompton,' Catherine Musinsky, · and Tomasz Owerkowicz'


Endothermy requires an integrated set of morphological and physiological features (Kemp 2006) that evolved independently in and (Ruben i996). Morphologic evidence for the of endothermy has partially been based upon the presence of the intranarial respiratory turbinals or conchae that act as temporal countercurrent exchange sites (Bennett and Ruben i986). Since endo­ therms have a higher respiratory rate than , evolution of the temporal countercurrent exchange mechanism allowed them to control the temperature of expired air when at rest and during mild exercise, and afforded them significant savings of heat and water (Owerkowicz et al., this volume). Birds achieved this by evolving cartilaginous nasal conchae (Bang i961; Geist 2000) , while mammals de­ veloped ossified maxillary turbinals (Macrini 2012; Rowe et al. 2005). Both mecha­ nisms warm and humidify inhaled air, and cool exhaled air (Schmidt-Nielsen i981), and both require a firm temporary seal between the and the , so that inspired and expired air passes through the nose and bypasses the oral

* Museum of Comparative , and Department of Organismic and Evolutionary , Harvard University t Department of Organismic and , Harvard University :j: Department of Biology, California State University, San Bernardino Monotremata Marsupialia P lacentalia 60 mya i f

In the gesting t mroughou To un nasal cap essary to 140 mya by them Haldl10do11 j MAMMALIA

to the s M orgal ucodon sal caps 200 mya Probai1rgnathus Masset[1ath11s J J

1hri11J_xodon 240 mya L CYNODONTIA

Dimr rodon


FIG . 11 .1 Relationships and timeline of the specimens discussed in this chapter

cavity. Conchae and maxilloturbinals also provide sites the three-boned , precise dental , for evaporative cooling during exercise and high ambi­ determinate growth, and an enlarged braincase-are ent temperatures (Taylor 1977). well documented. The evolution of the mammalian nose, Evolution of these countercurrent exchange sites however, remains relatively uncertain. Hillenius (1992, was likely gradual and probably involved considerable 1994), Hillenius and Ruben (2004), Ruben (1996), and reorganization of the skeleton. In this chapter, Ruben et al. (2012) have pointed to ridges found on the we focus on the evolutionary changes to the inner surface of the nasal and maxillary bones to sug­ skull, which may have housed the incipient respiratory gest that ossified turbinates were present in nonmam­ turbinates. malian . On the basis of these characters-the Within the nonmammalian therapsids (­ purported maxillary ridges, the presence of a bony like ) spanning more than 100 million years from secondary , and an enlarged nasal respiratory the mid- to the Early (fig. 11.1) (Kemp chamber-the authors concluded that several groups of 1982; Rowe and Gauthier 1992), some of the progressive nonmammalian therapsids were either partially or fully FIG. changes leading to the mammalian skull-for example, endothermic. of th

190 A . W . CRO MPTO N , CATHERINE M US INSKY, A ND T O MASZ OWERKOWI CZ In extant mammals the embryonic cartilaginous Jurassic mammaliaforms, and review important steps nasal capsule ossifies to form the mesethmoid and in the development of the mammalian nose. ethmoid bones. The latter include ossified maxi!lotur­ binals. But such ossifications have never been found Reptiles: Squamata in the nasal region of nonmammalian , sug­ gesting that the nasal capsule remained cartilaginous Olfaction is the primary function of the reptilian nose: throughout . olfactory nerves enter the posterodorsal region that lies To understand the structure of the cartilaginous above the flow of air through the nasal capsule. In typi­ nasal capsule of nonmammalian synapsids, it is nec­ cal living reptiles (Bellairs and Kamal 1981; Malan 1946; essary to determine the shape of the space enclosed Parsons 1959; Pratt 1948), a cartilaginous nasal cavity by the membrane bones that would have surrounded opens directly into the oral cavity through primary it. MicroCT scans contribute new insights to the find­ choanae, or internal nares (fig. 11.2.A, B); thus all air ings of Hillenius (1994), Ruben (1996), and Ruben et al. breathed through the nose must also pass through the (2012). Based on such scans, we offer suggestions as oral cavity. The route of air through the nasal capsule to the structure and function of some cartilaginous na­ between the nares and the primary is short (as sal capsules of nonmammalian and indicated by the arrow in fig. 11.2C), limiting the space

intern as al septum A B


pnmary choana

cartilaginous nasal capsule

primary Varner ~ choana Pterygoid Palatine

FI G. 11.2 Nasal region of an exta nt Amblyrhynchus cristatus (A- C) and an extinct limbotus (D). A, Transverse section; B, ventral view of the palate; C, sagittal section; D, sagittal section through the nasal region.

EVOLU T I O N OF THE M A MMAL I A N NOSE 191 for structures that might support respiratory epithe­ advanced nonmammalian therapsids suckled their lium. A tall, cartilaginous intemasal septum between young, possessed , and were endothermic. How­ the and the nasal roof separates the two sides of ever, this conclusion invites reexamination because the nasal cavity (fig. 11.2A). nonmammalian therocephalians had multiple genera­ tions of replacement throughout life, rather than the diphyodont of mammals, which correlates Early Nonmammalian Synapsids with rapid growth and early dependence on maternal In primitive nonmammalian synapsids, such as the for nourishment (Hopson 1973)· Dimetrodon (fig. 11.2D), the nasal capsule re­ mained cartilaginous. As in reptiles, the primary choa­ Nonmammalian Cynodonts nae open directly into the oral cavity (Hillenius 1992; Hillenius 1994; Romer and Price 1940), which limits the The description of the nasal capsule of nonmammalian space available to house structures supporting respira­ cynodonts given here is based upon MicroCT scans of tory epithelium. The posterior extent of a cartilaginous and the description nasal capsule is constrained by the presphenoid bone. of the skull of upon a reconstruction from The presphenoid is Y-shaped in cross-section, its ven­ serial grinding (Fourie 1974); and that of several cyno­ tral keel forms an interorbital septum and its expanded donts upon manually prepared (Brink dorsal area (Kemp 1980) encloses the olfactory nerves. 1955; Estes 1961; Hillenius 1992; Kemp 1980; Sues 1986). The dorsal edge of the tall pte1ygoid bone probably Advanced nonmammalian synapsids, such as the marks the ventral extent of the cartilaginous nasal cynodont Massetognathus, possess a fully ossified sec­ capsule. Given these volumetric constraints, the nasal ondary palate (fig. 1i.3B-E). The earliest presence of capsule of Dimetrodon was long, narrow, and, relative a in nonmammalian therapsids occurs in to the skull height, shallow. Several authors have sug­ nonmammalian cynodonts (Procynosu­ gested (see Hillenius 1992; Ruben et al. 2012) that ridges chus; Kemp 1979), and consists of medial projections of on the inner smiace of the intramembranous bones an­ the , maxilla, and palatine that do not meet terior to the presphenoid supported ossified olfactory in the midline. Thomason and Russell (1986) suggest turbinals. these played a mechanical function in resisting the It is generally accepted that were ec­ forces of mastication that probably arose with more tothermic (Hopson 2012; Kemp 2006). Therocephalian complex postcanine teeth. The median gap in the hard therapsids were more advanced than pelycosaurs in palate was probably occupied by soft tissue. that the dental row differentiated into well-defined inci­ The acquisition of a complete secondary palate co­ sors, canines, and small simple postcanines; however, incided with a major reorganization of the nasal region. their primary choanae did not increase much in rela­ In Massetognathus, the secondary palate formed the tive size and still opened directly into the oral cavity. floor of a nasopharyngeal duct. Primary choanae (dot­ Nonmammalian therocephalians lacked a hard ted lines in fig. 1L3B-D) opened into this nasopharyn­ palate, although Maier et al. (1996) claimed that ridges geal duct rather than straight into the oral cavity as in on the maxilla and palatine parallel to the postcanine reptiles and early nonmammalian synapsids. Air pass­ dentition supported choanal soft tissue folds that did ing through the nose could now bypass the oral cavity not meet in the midline. When their free edges were en route to or from the . pressed against the ventral surface of the vomer, a sec­ It is now possible to reconstruct the space that ondary palate was created that continued posteriorly would have contained the cartilaginous nasal capsule in the form of a mammalian muscular . This (fig. 11.4; fig. 11.sA, B). Unlike the long fiat bone presem would have allowed uninterrupted activity in the mouth in extant reptiles and nonmammalian pelycosaurs, the cavity without interfering with . Based upon vomer in Massetognathus extends dorsally as a vertical this interpretation, Maier et al. (1996) and Maier (1999) sheet of bone and divides the nasopharyngeal duct into claimed that nonmammalian therocephalians and more left and right regions (figs. 1L3B, C, 11.sA). The increase in



secondary choana pterygopalatine ridge A D 1 2 lateral ridge 1 2 (I ' 1 ~ Vom--- . -- Septomaxilla ~a 1 ~&1 maxillary ,./ ,.,canal premaxilla ~ I process incisal fora men l cm B

ll nasopharyngcal duct

FIG . 11.3 Nasal region of a nonmammalian cynodont (Massetognathus). Ventral view of the palate ( left) and transverse sections of the nasal cavity (A-E). Capital letters to the left of the palate indicate the position of the transverse sections shown in A-E. The two vertical lines la­ beled 1 and 2 indicate the planes shown in figure 11.SA and B.

height of this bone appears to have occurred as the pre­ by the palatine and vomer (fig. ii.3B- D). The posterior maxilla, maxilla, and palatine extended below the floor portion of the vomer forms a strut that, together with of the primary palate to form the hard secondary palate. the medially directed plates of the palatines, forms the Compared to those of primitive nonmammalian the­ anteri'or part of the transverse lamina (fig. 1i.3E) and the rapsids, Massetognathus and Probainognathus have floor to the posterior (olfactory) chamber of the nasal longer and wider primary choanae that extend back to cavity (fig. 11.5A, B). The grooved dorsal border of the the anterior edge of the primary palate (heretofore re­ vomer and the medial ridge on the ventral side of the ferred to as the "transverse lamina") (figs. ii.3E, 11.5B). in Massetognathus suggest the presence of The primary choanae are bordered laterally by the max­ a tall cartilaginous intemasal septum (figs. 1i.3B- E and illa and palatine, medially by the vomer, and posteriorly u.6D). The posterior extension of the primary choanae


nasopharyngeal maxillary passage antrum

FIG. 11. 4 Division of the nasal cavity as seen in dorsal and lateral views (see also supplementary video, Musinsky 2012, http://vimeo .com/43930404).

greatly increases the volume of a respiratory chamber cynodonts the ridges have a smooth surface, and no through which inhaled and exhaled air pass. Arrows in such fracture line is present. It is likely that the ridge on figure 11.5B indicate airflow through the primary choana the ventral edge of the nasal bone that Hillenius (1992) into the nasopharyngeal duct. claimed supported a respiratory turbinate in Massetog­ The internal surfaces of the membrane bones sur­ nathus is an artifact of dorsoventral compression be­ rounding the nasal cavity of Massetognathus have a se­ fore fossilization (Hopson 2012 contra Hillenius 1994). ries of ridges: a median ridge, two lateral ridges-one The medial ridge on the inner surface of the nasal bone on either side (fig. 1i.3C-E)- and one ridge on each in­ in Massetognathus almost certainly lay above a carti­ ner surface of the lacrimals and maxillae (figs. 1i.3C, D laginous internasal septum (fig. 1i.3C, D). This supports and 11.sA, B). These and some additional ridges have the view that the ridges on the inner surfaces of bones been described in several nonmammalian synapsids in the nasal region may, in fact, indicate the presence (Brink 1955, 1957; Fourie 1974; Hillenius 1994; Kermack of cartilaginous structures. Similarly, the lateral ridges et al. 1981). All these authors described these ridges as parallel to the median ridge may point to the presence the remnants of the bases of either ossified olfactory of cartilaginous nasal turbinals. However, we could find or respiratory turbinals. In modern mammals when the no ridges in the CT scans of Massetognathus that could maxilloturbinals are lost due to damage in dried skulls, indicate the number or orientation of cartilaginous a ridge terminated by a fracture line remains, indicat­ ethmoturbinals; so no attempt to reconstruct them ing the presence of maxilloturbinals. In nonmammalian has been made in figure 1i.3D or E. The long ridge that

19 4 A.W. CRO M PT O N , CATH ERINE MUSIN SKY, AND T OMASZ OWERKOWI CZ forms the base for the maxilloturbinals in mammals lies and n.6D). In reptiles, the nasal capsule does not ex­ close to the opening of the nasolacrimal duct (fig. n.6E). tend below the level of the dorsal border of the vomer The posterior edge of a similar ridge in Massetognathus (fig. n.2A) (Malan 1946); likewise, in Massetognathus (fig. n.5B) lies above the internal opening of the naso­ and other cynodonts the cartilaginous capsule probably lacrimal duct, suggesting that this ridge lies proximal to lay above the dorsal border of the tall vomer. Respira­ the base of a cartilaginous maxilloturbinal (figs. ii.3C, D tory turbinals may have filled the respiratory chamber

A orbitosphenoid E D c B A olfactory bulb respiratory chamber

lcm transverse B lamina opening lacrimal cl ct

cartilaginous cribriform plate c

I cm

FIG. 11 .5 A, Sagitlal and B, parasagittal sections through the snout of Massetognathus pascuali. C, Posterior view of the nasal region of the same specimen. Vertical lines labeled A through E indicate the position of the sections included in figure 11.3. The two vertical lines in figure 11.3 indicate the planes shown here in A and B.

EVOLUTION OF THE MAMMALIAN NOSE 195 above the large primary internal choana (fig. u.6D), with the lower , thus permitting more complex j w sugg but they may have extended ventrally into the naso­ movements (Crompton 1995)· The pterygoid hamul s unlil pharyngeal duct. We cannot calculate the surface area could be either a remnant of the large transverse pr~ · post of hypothetical respiratory turbinals, if they were in cess of the pterygoid of nonmammalian therapsids or the fact present, but since cartilaginous laminae tend to be a modification of the ectopterygoid (Barghusen 1986 . (will thicker than ossified turbinals, it is unlikely that their In mammals, the palatine and the pterygoid hamul s Olig surface area could have approached that of the highly form the roof and sidewall of a dome-shaped naso· an branched respiratory turbinals in many terrestrial and with a muscular soft palate as its floor. The haVI some aquatic mammals (Van Valkenburgh et al. 2011). palatopharyngeal muscle originates on the posterior bra Respiratory turbinates in mammals are effective at edge of the hard palate (palatine), hamulus, and sot s im controlling heat and water loss only if air to and from palate and extends backward around the larynx to in­ wit the can bypass the oral cavity (Biewener et al. sert in the dorsal wall of the pharynx (Crompton et al. ade 1985; Schmidt-Nielsen 1981; Taylor 1977). In mammals, 2008; Wood Jones 1940). The tensor veli palatini is po-1 et< a palatopharyngeal muscle extending from the hard and sitioned lateral to the pterygoid hamulus and extends soft (Wood Jones 1940) can surround the lar­ medially around the hamulus's ventral surface to insert ter ynx and tip of the and seal off from the oral in the anterior portion of the soft palate. The levator (fi! cavity the passage of air from the nasal capsule to the palatini runs ventrally to insert on the soft palate be­ thE trachea (Crompton et al. 2008) while the is ei­ hind the insertion of the tensor veli palatini. Barghusen bit ther mildly exercising or at rest. In most mammals the (1986) has shown that the tensor veli palatini and ten­ pa larynx remains in an intranarial position except during sor tympani muscles derived from the "reptilian" ptery­ lar swallowing, panting, or vocalization. Nothing is known goideus muscle. The former could only have inserted in! about the structure, position, or even the very pres­ on a soft palate by wrapping around the ventral margin ne ence of an intranarial larynx in nonmammalian synap­ of the transverse process of the pterygoid, and could fo· sids. Barghusen (1986) suggested that ridges extending only have achieved this once the transverse process no tli backward from the posterior edge of the hard palate to longer acted as a guide for lower jaw movement. Given Il\ the outer edge of the transverse process of the ptery­ these marked differences it is unlikely that the mamma­ J>} goid bone in nonmammalian cynodonts supported a lian arrangement of pharyngeal muscles or an intrana­ th non-muscular soft palate (shaded area in fig. ii.3). Bar­ rial larynx was present in nonmammalian cynodonts. fti ghusen (1986) further suggested that this would form The origin and development of mammalian pharyngeal the floor of a nasopharynx. Parallel pterygo-palatine musculature requires further study. ridges on the roof of the nasopharynx indicate two me­ Finally, temporal countercurrent exchange on turbi­ sl dial and two lateral channels (arrows, fig. 11.3)· The for­ nals works only if inspiration is quickly followed by ex­ ti mer, he proposed, led to the opening of the larynx and piration (Owerkowicz et al., this volume). This rhythm the latter to the medial surface of the of requires that a relaxed phase of breathing follows expi­ the lower jaw and a possible homologue of the mam­ ration (breathing out), when the lungs are in a deflated a malian auditory (Eustachian) tube. In all nonmamma­ state and the animal is momentarily apnoeic (not breath­ t lian cynodonts the transverse processes of the pterygoid ing). Such is the case in extant mammals, in which the r abut against the lower jaw, restricting jaw movement to relatively stiff ribcage and muscular diaphragm allow the sagittal plane. Barghusen (1986) claimed that a "rep­ maintenance of subatmospheric pleural pressure and tilian" pterygoideus muscle originated on the posterior prevent collapse of alveolar lungs. Hence, the ability to surface of the transverse processes and inserted on the conserve heat and water in the nasal cavity required the postdentary bones as it does in . presence of turbinals, but also depended on postcra­ The shape of the ventral surface of the palatine and nial . Klein and Owerkowicz (2006) argued pterygoid changed fundamentally between nonmam­ that the costal plates and thoracolumbar differentiation malian cynodonts and mammals. The transverse pro­ in Thrinaxodon point to the presence of a muscular cess of the pte1ygoid reduced in size and lost contact diaphragm before the origin of mammals, as originally

196 A.W. CROM PT ON, CATHERINE MUSI N SKY, A N O T OMASZ OWE RKOWICZ suggested by Brink (1955). We now find this scenario remained cartilaginous in Massetognathus and other unlikely, because other cynodonts do not show such cynodonts. postcranial morphology (Jenkins 1971; Kemp 1982), and The of the Middle to included the earliest record of a complex metameric arid to semiarid environments, as well as wet temperate (with sternebrae) is in the tritylodontids conditions with cool winters and warm summers (Prete (Ktihne 1956) and (Sues et al. 2010). Fauna included numerous diurnal nonmam­ and Jenkins 2006). The costal plates of Thrinaxodon malian cynodonts and early . Hopson (2012) have previously been interpreted to allow the animal to has characterized most nonmammalian cynodonts as brace the trunk against external forces (Jenkins 1971), "widely foraging" (WF), enabling carnivorous forms to similar to extant edentates (Jenkins 1970). This agrees search and hunt prey, and herbivorous forms to search a with a current interpretation of Thrinaxodon as an broad area for suitable vegetation. He concludes that WF adept burrower, adapted to habitats (Damiani nonmammalian cynodonts' low ex­ et al. 2003). ceeded the basal metabolic rate ofWF reptiles (e.g., vara­ The olfactory region of Massetognathus opens pos­ nids), and that they possessed a high maximum aerobic teriorly into the orbital region through a wide foramen necessary for sustained activity over long (fig. 11.5C). The frontal and postorbital form the roof of distances. It is doubtful that free-ranging nonmamma­ the foramen; the ventrally directed wings of the postor­ lian cynodonts could have maintained a constant body bital, the prefrontal, and the ascending lamina of the temperature if their basal metabolic rate was low. Diur­ palatine form its lateral borders; and the transverse nal mammals possess a high basal metabolic and breath­ lamina, its floor. All vessels and nerves enter­ ing rate, and maintain their body temperature slightly ing the nasal region passed through it. The maxillary above the average ambient temperature. This maintains nerve probably passed through this opening (fig. 11.5C), a temperature gradient for the loss of body heat to the forward through the maxillary canal and then through environment and minimizes the need for excessive evap­ the maxilla to exit onto the external surface through orative cooling when at rest or during mild exercise. On numerous small foramina (fig. 1i.3A, B), as it does in the other , maintaining a constant body temperature (Kemp 1979), Thrinaxodon, and several and breathing rate when the ambient temperature drops therocephalians (Estes 1961; Fourie 1974), rather than below the preferred body temperature requires insula­ from a large infraorbital foramen as in most extant tion, control of blood flow to the , and a mechanism mammals (Miller et al. 1968; Wible 2003). to control the loss of water and heat in the expired air. The Massetognathus orbitosphenoid is a long trough­ The structure of the palatine and pterygoid bones shaped bone, which joins the frontal to form a space for of nonmammalian cynodonts suggests that they did not the olfactory bulb (fig. 11.5A). The olfactory bulb opens possess the pharyngeal musculature to support an in­ into the posterodorsal aspect of the olfactory cham­ tranarial larynx, necessary to restrict the passage of re­ ber. In reptiles, embryonic mammals, and presumably spiratory airflow through the nasal cavity when at rest. It cynodonts as well (fig. 11.6A), the cartilaginous antor­ is, therefore, unlikely that cartilaginous maxilloturbinals bital plate forms the part of the posterior wall of the could have acted as temporal countercurrent exchange nasal capsule (Bellairs et al. 1981; De Beer 1937; Kuhn sites. Instead, turbinates could have provided a surface 1971; Zeller 1987) that lies below the entrance of the for evaporative cooling as they do during panting in olfactory nerves. In Massetognathus, the gap between mammals (ajr in through the nose and out through the the orbitosphenoid and the nasal cavity may have re­ mouth) when high levels of heat are generated during mained open as it does in reptiles and the exercise or when the ambient temperature exceeds the Omithorhynchus (De Beer 1937); or it may have con­ preferred body temperature. Evaporative cooling on the tained a cartilaginous cribriform plate as in embryonic surface of the maxilloturbinals of mammals have been Tacllyglossus (Kuhn 1971). An interorbital septum below shown to reduce body and brain temperatures (Taylor the orbitosphenoid, ossified in some other nonmam­ and Lyman 1972). We conclude that cartilaginous respi­ malian synapsids (Kemp 1972, 1969), appears to have ratory turbinals arose initially to aid in cooling and only

EVO LU T I O N OF T H E M A MMALIAN N OSE 197 later were co-opted to act as countercurrent exchang­ been suggested that they were nocturnal (Kemp 1982: ers when an intranarial larynx arose. Although adult hu­ Kielan-Jaworowska et al. 2004). If this is true and theij mans have lost the intranarial larynx, can seal the retained a combination of a low basal metabolic rate and entrance to the oral cavity and cause both inhaled and high aerobic metabolism, they may have been capable exhaled air to pass instead through the nasal cavity. of maintaining a low constant body temperature, as sev· eral nocturnal mammals such as and do, by combining a low basal metabolic rate and rest· Mammaliaformes ing body temperatures (Crompton et al. 1978). We agree Mammaliaforms such as the Late Triassic/Early Juras­ with Kemp (2006) that these extant secondar­ sic show several more mammalian na­ ily modified their metabolic rates to enter a nocturnal sal features. We MicroCT scanned the Morganucodon environment, but suggest that low basal metabolic and specimen (Institute of and Paleoanthro­ high maximum metabolic rates could have also been a pology, Beijing, #V8682) referred to in Rowe et al. (2011). strategy adopted by small nocturnal mammaliafonns The individual bones of this specimen are displaced and early mammals. and a reconstruction is currently being undertaken, The vacant space in the nasal cavity of Massctog· but the scans show a vomer dramatically reduced in nathus (fig. 11.6A, D) resembles the space that contains height, almost to mammalian levels, compared to non­ an ossified nasal capsule in the Didelpliis mammalian cynodonts. The much-flattened vomer no (fig. 11.6B-C, 11.6E-F). The embryonic nasal septum in longer divides the nasopharyngeal duct; consequently mammals ossifies to form the mesethmoid (fig. 11.6B, E) the respiratory chamber of the nasal capsule is much (Moore 1981). The compression of the vomer from a tall larger than in nonmammalian cynodonts. Kermack et al. bone in nonmammalian cynodonts to a thin splint of (1981) reconstructed the internal structure of the nasal bone lying below the mesethmoid increases the relative capsule of Morganucodon to include maxillary turbi­ size of the respiratory chamber, possibly allowing for nals, a cribriform plate and a mesethmoid bone. No evi­ increased space for ossified maxilloturbinals (fig. 11.6). dence of any of these ossified structures appear in our The posterior region of the embryonic cartilaginous MicroCT scans of Morganucodon. Perhaps the turbinals nasal capsule in mammals ossifies to form the ethmoid were too fragile to have remained intact before fossiliza­ bone that includes the ossified ethmoturbinals, naso· tion, but if the bulkier parts of the nasal capsule such as turbinals, and cribriform and lateral plates (Macrini the cribriform plate or the mesethmoid had ossified in 2012; Miller et al. 1968; Rowe et al. 2005). Morganucodon, surely some part of these bones would The ethmoturbinals occupy the chamber that fonns have been fossilized, especially as the remaining bones a blind alley above the transverse lamina, above and be· Fl of the skull are so well preserved. It appears, therefore, yond direct airflow from the nares to the nasopharyngeal n that in mammaliaforms the nasal capsule remained passage (fig. u.6C). This space in cynodonts undoubt· cartilaginous. edly also included olfactory turbinals that formed in the The orbitosphenoid and the olfactory bulb were, rel­ same way as they do in mammals-that is, as medial ex­ ative to skull size, considerably larger in Morganucodon tensions of the nasal capsule's cartilaginous side wall­ than in Massetognathus (Rowe et al. 2011). It is generally except that they remained cartilaginous. In embryonic agreed that some of the smaller mammaliaforms such as mammals tbe cartilaginous anterior region of the nasal r Morganucodon and had a diphyodont capsule appears close to the inner surface of the maxilla. dentition and definitive growth (Hopson 1973; Luo et al. During development, the ventral edges of the nasal cap 2004). Van Nievelt and Smith (2005) suggested that this sule extend into the nasal cavity. These and membranous indicated that these suckled their young because extensions later ossify to form maxilloturbinals, which in "the period of which requires no teeth elimi­ tum fuse directly to the maxillary bones (fig. n.6E). nates the need for functional replacement early during Maxilloturbinals branch repeatedly to create a large growth or at a small size." These animals were consider­ surface area, and are organized so as to reduce resis­ ably smaller than their nonmammalian ancestors. It has tance to the airflow to and from the nasopharyngeal

198 A.W. CROMPTON, CATHERINE MUSINSKY, AND TOMASZ OWERKOWICZ Orbito- cartilag_inous A sphenoid cribriform nasal D D late septum internasal septum respira --~-~ca~rtilagin ous turbinals ridge orbital septum maxi~ary atnum antorbital plate primary choana nasopharyngeal nasopharyngeal duct ~ duct

olfactory B bulb cribtiform --- late F E maxillary turbinal nasolacrimal duct


~ I 1 cm nasopharyngeal duct

Mesethmoid c F ethmoturbinal transverse lamina

basisphenoid presphenoid 1 ethmoid cm I hirhin~ 1 f G 11.6 Comparison of the nasal region of a nonmammalian cynodont, Massetognathus, and an extant basal mammal, Oidelphis. A, Sagittal tor through the nasal region of Massetognathus. Vertical line shows the position of the section shown in D; B, sagittal section through the al region of ; C, parasagittal section through the nasal region of Oidelphis, slightly lateral of B. Vertical lines indicate the position of sect ens shown in E and F.

duct. The long ridge that forms the base for the maxil­ The pterygoid bones of multituberculates are, as in loturbinals in mammals lies close to the opening of the all mammals, widely separated from the lower jaw. The naso-Jacrimal duct (fig. 11.6E). structure of the palatal region behind the hard palate in The first suggestion of ossified turbinals and a the multituberculate, Paulchojfatia delgao (Hahn 1987) mesethmoid bone appear in the mam­ is essentially mammalian, and suggests the presence in maliaforms docodont , as described by Lil­ mid-Jurassic mammals of pharyngeal muscles and an in­ ligraven and Krusat (1991). Although their paper does tranarial larynx. Fragments of bone have been described not distinguish between olfactory and respiratory turbi­ in the nasal cavities of the Late multitu­ nals, its authors claim that turbinals filled the nasal cav­ berculates, Nemegtbataar and (Hurum ay and that the foundations of some of these turbinal 1994). Hurum claims that these are the remnants of os­ ICl'Olls are preserved as ridges on the maxillae. sified turbinates. All three groups of living mammals-

EVOLUTION OF THE MAMMALIAN NOSE 199 ent nas eno hig Monotremata Ke1

Multituberculata Su M< im fol Haldanodon E ndothermy Intranasal larynx M organucodon Maxilloturbinals serve as sites for 1. temporal countercurrent exchange PE Probamognathus.~ O ssified maxilloturbinals? ar di '\ re Massetognathus Diphyodont n; Lactation & suckling rr D eterminate growth Reduction in number of tooth replacements. 2 Large respiratory chamber housing cartilaginous turbinals opens into nasopharyngeal duct, extended by a hard and n non- muscular soft palate. s r D ental row divides into , canines and postcanines

Cartilaginous nasal capsule Internal nares open into oral cavity Larynx opens into wide undifferentiated pharynx Undifferentiated tooth row with multiple replacements L ower jaw contacts large transverse processes of pterygoid

FI G. 11 .7 Progressive changes 1n the nasal, oral, and pharyngeal regions in nonmammalian synapsids.

, , and placentals (fig. 11.1)- creased compliance of the chest matching an increased possess ossified maxilloturbinals, so it is probable that volume of the nasal cavity, an intranarial larynx, and their common ancestor, which dates back to the Mid- ossified maxilloturbinals that can function either for dle Jurassic (Luo 2007), and probably existed alongside cooling or as temporal countercurrent exchange sites. some mammaliaforms (e.g., Haldanodon) , also possessed Conservation of water and heat represent only one fea- ossified maxilloturbinals and an intranarial larynx. ture necessary to support endoth ermy, but, we argue, Diurnal mammals have constant body temperature, maintaining constant body temperature in an environ- high basal and maximum aerobic metabolic rates, de- ment with significant shifts in daily and seasonal ambi-

2 0 0 A.W. CROMPTON, CATHERINE INSKY, AND TOMASZ OWER KOWI CZ ent temperatures would only have been possible when bulb was larger. A reduction in the height of the vomer nasal temporal countercurrent exchange sites were pres­ increased the relative volume of the respiratory cham­ ent together with other features necessary to support ber. Their diphyodont dentition suggests determinate

high basal and maximum metabolic rates (Hopson 2012; growth and suckling of their young. Kemp 2006).

4. Mammalia Summary and Conclusions The common ancestor of Mammalia probably had a Many questions remain about the successive changes muscular soft palate and a palatopharyngeal muscle involved in the evolution of the mammalian nose. The that could hold the la1ynx in an intranarial position. following steps are proposed (fig. 1i.7): The embryonic cartilaginous nasal capsule, including respiratory turbinates, completely ossifies in the adult. 1. Early Nonmammalian Synapsids This animal had a higher basal metabolic and breath­ ing rate than in typical reptiles and its maxilloturbinals, Permian nonmammalian pelycosaurs and therocephali­ operating as temporal countercurrent exchange sites, ans possessed a cartilaginous nasal capsule that opened controlled the loss of water and heat. Mammalian en­ directly into the oral cavity. This limited the space for dothermy arose when these changes in nasal structure respiratory turbinals within the airflow from the exter­ combined with a host of other specializations necessary nal nares to the primary choanae. They were ectother­ to support a high resting metabolic rate and constant mic, and the nose was designed primarily for olfaction. body temperature.

2. Nonmammalian Cynodonts Future Directions Nonmammalian cynodonts added a hard palate that may have been extended posteriorly by a non-muscular The conclusions reached in this paper are of necessity soft palate. Their respiratory chamber increased dra­ speculative due to the spotty record upon which matically in size. They probably lacked an intranarial they are based, an incomplete analysis of the internal larynx, and, if this is so, the path of respiratory airflow and external structures of critical regions in known during rest could not have been temporarily restricted , and the difficulty of relying on bony struc­ to the nasal cavity. Consequently, they lacked temporal tures alone for the reconstruction of soft tissues. Such countercurrent exchange sites for the conservation of shortcomings can be ameliorated in the future by us­ water and heat, necessary to maintain a constant body ing advanced imaging techniques to reexamine existing temperature and rhythmic breathing rate. However, material, and continuing field work to fill in gaps in the their cartilaginous maxilloturbinals and oral cavity pro­ fossil record, especially from the Early to Middle Juras­ vided surfaces for evaporative cooling during panting. sic, when the final steps in the occurred. Understanding the morphology of new speci­ mens will still require classic comparative anatomical 3. Mammaliaformes and physiological approaches aided by the study of the The structure of the nose in mammaliaforms appears to function and development of comparable regions in ex­ have been the same as in cynodonts, but the olfactory tant animals.



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