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Evolution of the Nasal Structure in the Lower Tetrapods

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Evolution of the Nasal Structure in the Lower Tetrapods AM. ZOOLOCIST, 7:397-413 (1967). Evolution of the Nasal Structure in the Lower Tetrapods THOMAS S. PARSONS Department of Zoology, University of Toronto, Toronto, Ontario, Canada SYNOPSIS. The gross structure of the nasal cavities and the distribution of the various types of epithelium lining them are described briefly; each living order of amphibians and reptiles possesses a characteristic and distinctive pattern. In most groups there are two sensory areas, one lined by olfactory epithelium with nerve libers leading to the main olfactory bulb and the other by vomeronasal epithelium Downloaded from https://academic.oup.com/icb/article/7/3/397/244929 by guest on 04 October 2021 with fibers to the accessory bulb. All amniotes except turtles have the vomeronasal epithelium in a ventromedial outpocketing of the nose, the Jacobson's organ, and have one or more conchae projecting into the nasal cavity from the lateral wall. Although urodeles and turtles possess the simplest nasal structure, it is not possible to show that they are primitive or to define a basic pattern for either amphibians or reptiles; all the living orders are specialized and the nasal anatomy of extinct orders is unknown. Thus it is impossible, at present, to give a convincing picture of the course of nasal evolution in the lower tetrapods. Despite the rather optimistic title of this (1948, squamates), Stebbins (1948, squa- paper, I shall, unfortunately, be able to do mates), Bellairs and Boyd (1950, squa- iittle more than make a few guesses about mates), and Parsons (1959a, reptiles). Most the evolution of the nose. I can and will of the following descriptions are based on mention briefly the major features of the these works, although others, specifically nasal anatomy of the living orders of cited in various places, were also used. amphibians and reptiles, but all of these Further references may be obtained from are more or less specialized. Truly primitive the bibliographies given by Matthes (1934), amphibians and reptiles are known only Parsons (1959a), and the other papers as fossils and, since the nasal capsules are cited. virtually never ossified in them, their nasal In the following descriptions and discus- anatomy cannot be studied directly. It is sion I shall limit myself to a consideration possible to attempt working back to a com- of the structure of the nasal cavities with mon and hopefully primitive pattern from brief comments on their innervation and the living forms, but such an attempt is development. The structure of the nasal dangerous since it generally involves un- capsule and the nasal physiology with its likely assumptions, e.g., that the loss of behavioral aspects are also important for structures is uncommon and that secondary any complete understanding of nasal evo- simplification is rare. lution, but time does not permit their con- The literature on the nose is extensive. sideration here. Before describing the vari- The most important review is that by ous groups I should first review the major Matthes (1934). Other major works include subdivisions and structures of the tetrapod those of Sarasin and Sarasin (1887-1890, nose. gymnophionans), Seyclel (1895, amphi- bians; 1896, turtles), Hoppe (1934, rhyn- MAJOR NASAL STRUCTURES chocephalians), Schuch (1934, urodeles), The nasal cavities of most tetrapods may Bertau (1935, crocodilians), Helling (1938, anurans), Malan (1946, squamates), Pratt be divided into three main parts. In most cases the largest is the central cavum nasi I wish to thank Dr. Margaret C. Parsons for proprium, a variably shaped but typically her assistance in the preparation of this manuscript. enlarged cavity which is lined, in part, by Some of the work reported here was supported by Grant A-1724 from the National Research Council the sensory olfactory epithelium. Anterior of Canada. to this, between it and the external naris, (397) 398 THOMAS S. PARSONS there may be a more or less tubular the nasal cavity which forms a distinct vestibulum. The latter is often lined by sensory structure; in many cases it becomes squamous epithelium resembling the epi- associated with the oral cavity of the adult dermis and is sometimes said to be formed and loses its connection with the nasal from epidermal epithelium rather than cavity. Other workers, most notably Seydel from epithelium derived from the nasal (1895 and 1896), have considered not only placode of the embryo, but these characters such distinct outpocketings to be the are variable or difficult to determine; thus, Jacobson's organs, but also areas of sensory epithelium presumably homologous to the term vestibulum is here used in a gross Downloaded from https://academic.oup.com/icb/article/7/3/397/244929 by guest on 04 October 2021 morphological sense referring to any more- them in forms that lack such outpocketings. or-less tubular connection between the ex- Their homology is recognized by three ternal naris and the main portion of the main characters: first, the sensory epitheli- nasal cavity. Posterior to the cavum nasi um of Jacobson's organ in the broad sense proprium there is commonly another tu- lacks Bowman's glands while these glands bular portion, the nasopharyngeal duct, are present in the olfactory epithelium of leading to the choana or internal naris. virtually all tetrapods (neotenic urodeles Some authors restrict the term naso- and one genus of sea snakes are the only pharyngeal duct to the channel dorsal to a known exceptions); second, the olfactory well-formed secondary palate, but I will nerve fibers from jacobson's organ tend to here use it for any posterior tubular lead to the accessory olfactory bulb while portion of the nasal cavity and will not, at those from the olfactory epithelium lead to this time, consider the very extensive the main olfactory bulb; and, third, Jacob- literature on the types of palates in reptiles son's organ tends to be ventrally located and their relationships to the nasal cavities while the olfactory epithelium lies mainly in the dorsal parts of the cavum nasi pro- (for reviews of this topic see the papers of prium. Although in this paper I shall use Fuchs, 1915, and Parsons, 1959a). Either the first and more restricted definition of the external naris or the choana may enter Jacobson's organ, I wish to emphasize the the cavum nasi proprium directly in which homology of that organ with those regions case the vestibulum or the nasopharyngeal lined by sensory epithelium which meets duct is not present. the three criteria presented above. Such epi- Projections of the lateral nasal wall of thelium is here termed vomeronasal epithe- the cavum nasi proprium (or, more rarely, lium in contrast to the remaining types of of the vestibulum) into the nasal cavity are epithelia found in the cavum nasi propri- termed conchae. Although Gegenbaur um, sensory olfactory epithelium and non- (1873) and de Beer (1937) have proposed sensory respiratory epithelium. In no case different and even mutually exclusive does a tetrapod possess both a true Jacob- definitions in an attempt to give greater son's organ and other areas of vomeronasal precision to this term, I prefer to use epithelium within the nasal cavity. concha in a general sense. Neither of the restricted definitions assists in the re- SARCOPTERYGIAN FISHES cognition of homologies nor even of gen- eral structural similarities and the more Since the sarcopterygian fishes are uni- general usage of the term is convenient versally accepted as the ancestors of the (see Parsons, 1959a, for a discussion of tetrapods, it seems logical to start a discus- these definitions). Conchae are found only sion of the evolution of tetrapod noses with in amniotes. a few words on their nasal anatomy. Un- The Jacobson's or vomeronasal organ is fortunately, however, such a procedure tells frequently an important accessory olfactory us essentially nothing about the nasal organ in tetrapods. It has been defined in cavities of the most primitive land forms. two different ways. Some authors restrict The best known sarcopterygians are the the term to a ventromedial outpocketing of lungfish; they have been described most TETRAPOD NASAL STRUCTURE 399 recently by Bertmar (1965 and 19666) and presence and, to a certain extent, the shape Thomson (1965). In the Dipnoi the nasal of a Jacobson's organ in some rhipidistians, cavities are basically like those of most but, on the basis of Thomson's study, I feel other fish and show few, if any, tetrapod that any such identification of Jacobson's characters. They are relatively simple sacs organ must be considered extremely ten- with numerous olfactory folds or lamellae. tative although quite possibly correct. In Although the posterior nostril does open any event the uncertainty is great enough into the oral cavity, there is general agree- to make further speculation on rhipidistian ment that this opening does not correspond noses unprofitable for the purposes of this Downloaded from https://academic.oup.com/icb/article/7/3/397/244929 by guest on 04 October 2021 to the choana of tetrapods, a structure com- paper; for detailed descriptions, specula- pletely lacking in the lungfish. Various tions, and references, see the papers by workers have described different parts of Jarvik (1942) and Thomson (1964). the dipnoan nasal cavity as a Jacobson's organ, but Bertmar (1965) has shown that URODELA there is no evidence for the existence of any The nasal cavities of many urodeles are such organ in lungfish except, possibly, for very simple (Fig. 1). There is little or no Rudebeck's (1944) report of a rudimentary vestibulum and no nasopharyngeal duct. accessory olfactory bulb. I am unconvinced In most forms, such as Triturus and Sala- by Rudebeck's description and doubt that mandra, the cavum nasi proprium consists an accessory bulb is present.
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