Ancestral loss of the maxillary sinus in Old World monkeys and independent acquisition in Macaca.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 117:293–296 (2002) Ancestral Loss of the Maxillary Sinus in Old World Monkeys and Independent Acquisition in Macaca Todd C. Rae,1* Thomas Koppe,2 Fred Spoor,3 Brenda Benefit,4 and Monte McCrossin4 1 Evolutionary Anthropology Research Group, Department of Anthropology, University of Durham, Durham DH1 3HN, UK, and Department of Mammalogy, American Museum of Natural History, New York, New York 10023 2 Institut für Anatomie, Ernst Moritz Arndt Universität Greifswald, D-17487 Greifswald, Germany 3 Evolutionary Anatomy Unit, Department of Anatomy and Developmental Biology, University College London, London WC1E 6JJ, UK 4 Department of Anthropology, Southern Illinois University, Carbondale, Illinois 62901 KEY WORDS cranial pneumatization; Cercopithecoidea; Macaca; character state evolution ABSTRACT Cercopithecoid monkeys are unique among primates in that all species (except macaques) lack a maxillary sinus, an unusual condition among eutherian mammals. Although this uncommon distribution of cranial pneumatization was noted previously, the phylogenetic ramifications have not been investigated fully. Recently, character state optimization analysis of computed tomography (CT) data from extant Old World monkeys suggested that the loss of the sinus may have occurred at the origin of the group, unlike previous hypotheses positing only a reduction in size of the structure. To critically evaluate the “early loss” hypothesis, a recently recovered complete cranium of Victoriapithecus macinnesi from Maboko Island, Kenya, was examined by CT to determine the extent of its cranial pneumatization. This taxon is crucial for evaluating character state evolution in Old World monkeys, due to its phylogenetic position, preceding the cercopithecine/colobine split. CT analysis reveals only cancellous bone lateral of the nasal cavity, indicating that Victoriapithecus does not possess a maxillary sinus. Phylogenetic evaluation of the fossil with extant catarrhine taxa strongly supports the early loss of the sinus in cercopithecoids. The results suggest that the maxillary sinus found in the genus Macaca is not homologous with that of other eutherians, which may provide insights into the origin and function (if any) of the paranasal pneumatizations. Am J Phys Anthropol 117: 293–296, 2002. © 2002 Wiley-Liss, Inc. The crania of most mammals include some form of paranasal pneumatization invading the bones surrounding the nasal cavity proper. These bony air cells are produced in growth by the advancement of osteoclastic epithelial diverticulata; the resulting sinuses are found in the facial skeleton of both eutherian mammals and archosaurs (Witmer, 1999). Although paranasal pneumatization was described in the scientific literature as early as 1651 (Koppe et al., 1999a), the biological role of the paranasal sinuses remains unclear (Blanton and Biggs, 1969; Blaney, 1990; Witmer, 1997). This ambiguity may be due, in part, to a lack of understanding of the phylogenetic distribution of sinuses across taxa. Although some primate taxa have as many as four separate pneumatized loci in the facial skeleton, the most common of these bony air spaces is the maxillary sinus (MS). This structure is housed primarily in the maxilla and opens into the nasal cavity via an ostium (hiatus semilunaris) in the middle meatus, above the inferior nasal concha. Cranial pneumatization among extant taxa indicates that the MS is primitive for eutherian mammals (Novacek, 1993). Primates display a distribution similar to other eutherians (Paulli, 1900); the MS is widespread across the order, and other sinuses (frontal, sphenoidal, and ethmoidal) are less common (Koppe and Nagai, 1998). Cercopithecoid monkeys, on the other hand, are unique among anthropoids with respect to the distribution of the MS. Unlike hominoids (Cave and Haines, 1940) and platyrrhines (Koppe et al., 1999c), most extant cercopithecoids completely lack maxillary pneumatization (Paulli, 1900; Ward and Brown, 1986; Rae, 1999). Figure 1 shows coronal CT scans through the face of Cercocebus torquatus; the area between the nasal cavity and the outer table of bone of the maxilla is filled with spongy bone. MS loss is not unique to cercopithecoids; other mammalian taxa have been reported to lack the structure as well (Moore, 1981; Novacek, 1993). © 2002 WILEY-LISS, INC. Grant sponsor: Leakey Foundation; Grant sponsor: Royal Society; Grant sponsor: University of Durham. *Correspondence to: Todd C. Rae, Department of Anthropology, University of Durham, 43 Old Elvet, Durham DH1 3HN, UK. E-mail: firstname.lastname@example.org Received 14 December 2000; accepted 2 August 2001. DOI 10.1002/ajpa.10008 Published online in Wiley InterScience (www.interscience.wiley. com). 294 T.C. RAE ET AL. Fig. 1. Representative coronal CT scans of Cercocebus torquatus, at level of premolars (left), first molar (center), and third molar (right). Black spaces in the maxilla in the scan at left are canine alveoli. The bone lateral of the nasal aperture is cancellous, showing no sinus space. Fig. 2. Representative coronal CT scans of Macaca fascicularis, as in Figure 1. The maxillary sinus can clearly be seen lateral of the nasal cavity as far back as M3. Macaca is the only cercopithecoid known to date to possess a paranasal pneumatization in the maxilla. The lack of the MS, however, is not uniform within Old World monkeys; the genus Macaca, alone among the cercopithecoids examined to date, possesses a well-developed sinus space in the maxilla (Koppe and Ohkawa, 1999). Figure 2 shows the large sinus space in the maxilla of M. fascicularis, which is comparable in size (relative to size of the cranium) to that seen in hominoids and platyrrhines (Koppe and Nagai, 1999). In addition, unlike the condition seen in hominoids (Rae and Koppe, 2000) and probably platyrrhines (Koppe et al., 1999c), there is only a weak relationship between cranial size and sinus volume in macaques (Koppe and Nagai, 1998), perhaps due to environmental influences (Rae et al., 1997). Phylogenetic analysis of cranial pneumatization in extant cercopithecoids reveals a surprising conclusion: the best-fit optimization of character state change on a well-supported cladogram of Old World monkeys suggests that the MS was lost early in cercopithecoid evolution, before the cercopithecine/colobine split (Rae, 1999). This “early loss” hypothesis differs from previous suggestions of MS reduction in early cercopithecoids (Harrison, 1987; Rae, 1997), and implies that extant macaques have undergone an evolutionary re- Fig. 3. Representative coronal CT scans of Victoriapithecus macinnesi, as in Figure 1. Matrix is present in both the orbits and the nasal cavity. As with Cercocebus (Fig. 1) and all nonmacaque cercopithecoids, there is no paranasal pneumatization in the maxilla. (The black area at left on the M3 scan at far right is caused by the cranium being somewhat oblique in the scanner; this resulted in the signal passing through the slight concavity at the back of the zygomatic.) versal to “regain” a sinus in the maxilla, a unique event in eutherian evolution. The early loss hypothesis of the Old World monkey MS is subjected to a critical test here by CT examination of the stem cercopithecoid Victoriapithecus macinnesi. This taxon is crucial to hypotheses of evolutionary change in Old World monkeys, due to its status as the sister taxon of extant cercopithecids, having diverged prior to the last common ancestor of cercopithecines and colobines (Benefit, 1987, 1993). Previous observations on broken and incomplete specimens suggested that the maxilla of Victoriapithecus was not pneumatized (Benefit and McCrossin, 1993), but no complete specimens had been recovered until recently. MATERIALS AND METHODS The discovery of KNM MB 29100, a complete cranium of Victoriapithecus macinnesi from the ca.15-Ma deposits of Maboko Island, Kenya (Benefit and McCrossin, 1997), allows, for the first time, the unequivocal evaluation of cranial pneumatization in a stem cercopithecoid. The specimen includes complete and undistorted maxillae on both sides of the nasal cavity. To evaluate the internal structure of the cranium in a non-invasive fashion, CT was employed. This technique is especially useful in the case of fossils such as MB 29100, where the nasal cavity is partially filled with matrix. Coronal CT scans were made with the Siemens Somatom AR.SP of the MITC Diagnostic Centre, Nairobi, at 130 kV, 249 mAs, with slice thickness and increment of 1 mm, and a pixel size of 0.17 mm. The resulting character state data were evaluated using the optimizations provided in the cladistic software package Hennig86 (Farris, 1988). RESULTS Figure 3 shows representative coronal CT scans through the maxilla of MB 29100. There is good image contrast between bone and the matrix in the nasal EVOLUTION OF MAXILLARY SINUS IN CERCOPITHECOIDS Fig. 4. Phylogenetic reconstruction of sinus evolution in Old World monkeys. The lack of a sinus in the maxilla of Victoriapithecus confirms the inference (Rae, 1999) that cercopithecoids lost the MS early in their evolution, and that macaques subsequently regained the structure. cavity. Small, less dense areas above the molar roots are clearly matrix-saturated cancellous bone, separated from the nasal cavity at all levels by a welldefined and uninterrupted bony wall. All of the bone lateral of the nasal cavity proper at the level of the molars (the only area pneumatized in macaques) is cancellous; there is no sinus space, nor is there an ostium in the middle meatus. In all aspects, the maxilla of Victoriapithecus resembles that of Cercocebus (Fig. 1) and all other nonmacaque cercopithecoids, and does not possess a maxillary sinus. The lack of MS in the fossil strongly supports the interpretation of the complete absence of the MS in the last common ancestor of the living subfamilies (Colobinae, Cercopithecinae). Character optimization on a well-supported topology (Strasser and Delson, 1987) suggests that the stem lineage of the group possessed no maxillary pneumatization (Fig. 4). This observation effectively falsifies any reconstructions that posit the presence of the MS as primitive for Old World monkeys, even if described as laterally restricted/small (Rae, 1997) or relatively/ very restricted (Harrison, 1987). In addition, the new data also support the hypothesis that the MS has evolved independently in macaques. DISCUSSION Although many workers have noted the lack of MS in many species of cercopithecoid monkeys (Paulli, 1900; Hershkovitz, 1977; Ward and Brown, 1986), the conclusion that ancestral cercopithecoids lacked paranasal pneumatization of the maxilla makes the group unique among mammals. A few other mammalian taxa are reported to have lost the MS, but many of these cases have obvious explanations, such as size in small bats (Novacek, 1993) or adaptation to marine environments in cetaceans (Moore, 1981). 295 The early loss of the sinus in cercopithecoids offers no such simple solution. One possible determinant for reduction of the MS, temperature, is not applicable in the present case. It has been reported that the sinuses of both humans (Shea, 1977) and macaques (Rae et al., 1997) are reduced in size at higher latitudes, probably due to a corresponding increase in size of the nasal cavity. The earliest cercopithecoids, however, are known exclusively from tropical to subtropical environments, as are all but two extant species. The geographic placement of the early cercopithecoids makes it unlikely that extremes in temperature were responsible for the loss of the MS. Interestingly, both of the Old World monkeys whose ranges lie in temperate regions (Macaca mulatta, M. fuscata) posses a sinus space in the maxilla, although it is relatively smaller than that found in their tropical congeners (Koppe and Ohkawa, 1999). Since successive outgroups of Macaca lack the structure, it is evident that the air space in the maxilla of macaques is not homologous with the maxillary sinus sensu stricto (Fig. 4), even though the anatomical conformation of the structure is identical with that seen in other primates (Paulli, 1900; Ward and Brown, 1986; Koppe and Ohkawa, 1999). This remarkable convergence offers a unique opportunity to investigate the possible selection pressure(s) responsible for the origin of this pneumatic space, since current data suggest that all other mammalian taxa that possess a maxillary sinus (including other primates) inherited it from a common eutherian ancestor (Novacek, 1993). The inference of a unique convergence in the MS highlights the importance of phylogenetic information for explanations of the evolution of morphological characters. It is only the study of character change across clades that can determine the events that require explanation. This is an essential step to avoid unnecessary rationales for morphology. For example, the answer to the oft-repeated question, “Why do humans have maxillary sinuses?” (see, for example, Blaney, 1990) is that their ancestors had them. As has been known for some time (Cave and Haines, 1940), all great apes (including humans) possess the character, as do most eutherian mammals, making it most likely that the character was present in the common ancestor of all hominoids and was simply retained in humans. As such, the presence of the sinus (independent of utility; see below) in Homo sapiens does not require explanation beyond phylogeny. It is only those instances where characters can be shown to have changed at a particular node that require special interpretation, usually as an adaptation. This argument is implicit in criterion 3 of Kay and Cartmill (1977) for inferring function; the character must not have preceded the usage evolutionarily. Witmer (1997) explains that we “may readily accept the idea that the . . . [avian] sinus is just another ‘adaptation for reducing the weight of the skull for flight’ . . . [but] a homologous 296 T.C. RAE ET AL. structure was present before any archosaurs took to the air, and thus the historical genesis of the sinus was not as a flight adaptation.” As Sheridan demonstrated with Dr. Pangloss, current utility is not a foolproof reflection of past selection pressure. It is essential to investigate the point of origin to understand the “reason” for the evolution of a structure. Thus, the discovery of the evolutionary reemergence of the maxillary sinus in macaques may have a bearing on the inference of the function (if any) of the paranasal sinuses, an area of considerable debate at present (Koppe et al., 1999b). Most of the previously suggested hypotheses to explain the presence of pneumatic spaces in the cranium rely heavily on current utility (Witmer, 1997). The pattern of sinus evolution in cercopithecoids outlined above provides two previously unavailable evolutionary phenomena: an ancestral loss with no immediately obvious explanation, and the independent origin of the structure in a well-studied group of organisms that may be as little as 6 Ma old (Szalay and Delson, 1979). By identifying the precise nodes at which these evolutionary changes occurred, the present study has identified new areas of exploration that may be instrumental for inferring both the proximal causes of the origin and loss of sinus spaces in the primate cranium and (possibly) the biological role of cranial pneumatization in Mammalia. ACKNOWLEDGMENTS The authors thank the Governors of the National Museums of Kenya (M. Leakey, N. Adamali, B. Sokhi, and F. Kirera) and the Permanent Secretary, Ministry of Education for permission to study materials and for help with CT scanning, and three anonymous reviewers. LITERATURE CITED Benefit B. 1987. 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