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The Paranasal Sinuses of Higher Primates Development, Function, and Evolution

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The Paranasal Sinuses of Higher Primates Development, Function, and Evolution Thomas Koppe / Hiroshi Nagai / Kurt W. Alt The Paranasal Sinuses of Higher Primates Development, Function, and Evolution Special Reprint The Phylogenetic History of Paranasal Air Sinuses Lawrence M. Witmer Chapter 2 The Phylogenetic History of Paranasal Air Sinuses Lawrence M. Witmer Paranasal air sinuses have long been fossil record is often critical in bridging of great interest to anatomists working morphologic gaps observed in the extant on mammals in general and primates realm, and a phylogenetic perspective in particular; clinically oriented human dictates which are the most appropriate anatomists probably have generated the paleontologic comparisons. largest proportion of the literature. Paranasal pneumaticity, however, is not restricted to mammals, and numerous other clades of vertebrates exhibit air-filled Definitions epithelial diverticula of the nasal cavity. Although paranasal sinuses in nonmam­ Before the distribution of pneumatic struc­ malian vertebrates often have been given tures throughout vertebrates can be the names of their presumed mammalian examined, a few concepts must be clari­ counterparts, the homologies of some of fied. The first is the distinction between a these sinuses have only recently been soft tissue pneumatic diverticulum and subjected to scrutiny (Witmer, 1995b). the bony recess that often houses it. The Progress in interpreting the diversity of term sinus has been applied to both, and, vertebrate sinuses historically has been for many questions, the distinction is not hampered by typologie approaches that that important. However, it often is crucial have sought to homologize mammalian in comparisons across broad taxonomic (principally human) sinuses with those of groups. For example, an epithelial diver­ other vertebrates under the often unstated ticulum may be present in numerous taxa, belief that all organisms will display mani­ but only pneumatize bone in a subset of festations of the archetype. A phyloge­ these taxa, an example being the subor­ netic perspective, however, improves bital diverticulum of the antorbital sinus in prospects for successful interpretation of birds and some other archosaurs (Witmer, sinus diversity, in that it provides for a bet­ 1997). Likewise, very similar bony recess­ ter sense of what is truly homologous, es may result from pneumatization via dif­ which in turn provides the appropriate ferent pneumatic diverticula (Witmer, framework for functional and other infer­ 1990), thus presenting problems of ences. Furthermore, evidence from the homology. Perhaps most fundamentally, 21 The Phylogenetic History of Paranasal Air Sinuses diverticula and bony recesses stand in nasal cavity proper. However, in those morphogenetic relation to each other as nonmammalian vertebrates eXhibiting cause and effect; that is, in most if not all paranasal pneumaticity, diverticula arise cases, the bony recesses are actually pro-­ not only from the nasal cavity proper, but duced through pneumatization via the also from the other portions of the cavitas epithelial diverticulum and its osteoclastic nasalis. Thus, although mammals gener­ front (Witmer, 1995a, 1997). ally have extensive paranasal sinuses, the Another distinction must be made morphogenetic diversity of sinuses in between intracapsular and extracapsular mammals is less than in some other ver­ recesses. Intracapsular recesses are tebrate clades. those internal to the cartilaginous nasal capsule, and, although their names some­ times sound like pneumatic recesses (eg, Mihalkovics' [1898] identification of a Phylogenetic Distribution of "sinus maxillaris" in the lizard Lacerta), it Paranasal Sinuses appears that only epithelial diverticula that have escaped the bounds of the cartilagi­ The literature on the phylogenetic distrib­ nous capsule (that is, extracapsular sinus­ ution of sinuses is widely scattered es) are competent to pneumatize bone among the primary literature. Summary (Witmer, 1995b). In many clades of verte­ information can be found in comparative brates, the nasal capsule is not a com­ anatomic texts, especially older ones, plete cartilaginous box, but rather has var­ such as Dieulafe (1905a, 1905b, 1905c, ious openings (in addition to the nares 1905d), Plate (1924), and Matthes (1934), and choanae) that may transmit evagina­ among others. Nemours (1930a, 1930b) tions of nasal epithelium, allowing, in published two rather naive and very typo­ effect, intracapsular epithelium to logic reviews on the status of the become extracapsular. As discussed later paranasal sinuses of modern amphibians, in this chapter, some of these outpocket­ reptiles, and birds. Negus (1958) pub­ ings bear some histologic resemblance to lished .an extensive comparative treatise pneumatic diverticula, but only a few that provides excellent information on actually pneumatize bone. mammals but only superficial coverage of A final point of clarification relates to the nonmammalian vertebrates. The closest site of origination within the nasal cavity of thing to a modern review is Witmer's the pneumatic diverticulum. Parsons' (1995b) study of facial anatomy of (1970) division of the nasal cavity is useful archosaurs, which reviews much of the in this regard. He divided the nasal cavity previous literature on other extant into the vestibule rostrally, the nasal cavity amniotes. This chapter is intended only as proper (cavum nasi proprium) in the mid­ an overview, and there are a number of dle, and the nasopharyngeal duct caudal­ areas that require much more in-depth ly. In primates, as in apparently all mam­ study. In the following survey, vertebrate mals (Paulli, 1900a, 1900b, 1900c; taxa will be taken in turn, roughly following Moore, 1981), all of the various paranasal the pectinate cladogram topology of Fig sinuses originate as diverticula of the 2-1. 22 Phylogenetic Distribution of Paranasal Sinuses of why some paranasal diverticula pneu­ matize bone and others do not. Given this situation, it would be of interest to survey fossil material of the large-skulled "reptil­ iomorph" nonamniote anthracosaurs to seek evidence of paranasal sinuses. Amniota Despite any prospects for the discovery of paranasal air sinuses in nonamniote ver­ tebrates, it remains that paranasal pneu­ maticity is still known only in amniotes. Tetrapoda However, as discussed in detail elsewhere Fig 2-1 Phylogenetic relationships of extant (Witmer, 1995b), it appears that the pres­ tetrapods. (Topology after Gauthier et aI., 1988.) ence of paranasal sinuses is not a synapo­ morphy of Amniota. Rather, pneumaticity evolved independently at least twice-in Mammalia and Archosauria-and, in each case, numerous different paranasal sinus­ es evolved. The following will be a very Nonamniote vertebrates brief survey of the major clades of amni6tes (see Fig 2-1), examining their To my knowledge, bony pneumatic various epithelial diverticula and bony recesses have not been reported in any pneumatic recesses, when present. extinct or extant nonamniote vertebrate (i.e., fishes and amphibians), a finding that Mammalia is perhaps not too surprising, given the aquatic habits of most of these animals. Paulli's (1900a, 1900b, 1900c) masterful However, the potential for pneumatization work on mammalian paranasal pneu­ of bone would seem to be present in maticity remains the primary reference some modern amphibians, in that extra­ and was the basis for most of the recent capsular epithelial diverticula have been reviews (Moore, 1981; Novacek, 1993), described and/or illustrated for various although Negus (1958) also provided salamanders and especially frogs by some novel Observations. According to Mihalkovics (1898), Plate (1924), Ne­ these sources, monotremes and marsupi­ mours (1930a), Matthes (1934), and als (with perhaps a single exception) lack Jurgens (1971), among others. paranasal sinuses of any kind. Fur­ These diverticula appear in section (Fig thermore, among eutherians (i.e., placen­ 2-2A), to be generally similar to the diver­ tal mammals), only the maxillary sinus is a ticula that pneumatize bone in amniotes, nearly ubiquitous feature. (It is absent in a but they do not do so, raising the question few small bats [Novacek, 1993] and most 23 The Phylogenetic History of Paranasal Air Sinuses A nasal capsule B nasal cavity vestibule proper bone nasal cavity proper ....-;:;;;/~'l'/~;;!'; o bone C recessus ducti nasopharyngei nasal nasal cavity nasal nasal cavity capsule proper capsule proper Fig 2·2 Extracapsular epithelial diverticula without pneumatization of bone in (A) the anuran amphibian, Hy/a arborea (transverse section); (8) the turtle, Testudo graeca (sagittal section); (e) the turtle, Emys eumpaea (transverse section); and (D) the squamate lepidosaur, Varanus ni/oticus (transverse section). Pneumatization of bone requires the evagination of a thin-walled epithelial diverticulum beyond the bounds of the cartilaginous nasal capsule. The taxa shown have such a diverticulum, but it fails to pneumatize bone. In Varanus, the diverticulum has been named the recessus extracapsu/aris (Malan, 1946), whereas in turtles it is known as the recessus ducti nasopharyngei. (A) Modified from Mihalkovics (1898). (8) Modified from Parsons (1970) and Witmer (1995b). (C) Modified from Mihalkovics (1898). (D) Modified from Malan (1946). marine mammals [Moore, 1981]). It ap­ from the olfactory region of the nasal cav­ pears that all of the eutherian maxillary ity. This system may be best termed the sinuses are homologous, although a rig­ ethmoidal sinus system, although the orous test
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