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Ancestral loss of the maxillary sinus in Old World monkeys and independent acquisition in Macaca.

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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
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
Institut für Anatomie, Ernst Moritz Arndt Universität Greifswald, D-17487 Greifswald, Germany
Evolutionary Anatomy Unit, Department of Anatomy and Developmental Biology, University College London,
London WC1E 6JJ, UK
Department of Anthropology, Southern Illinois University, Carbondale, Illinois 62901
cranial pneumatization; Cercopithecoidea; Macaca; character state evolution
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,
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).
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.
Received 14 December 2000; accepted 2 August 2001.
DOI 10.1002/ajpa.10008
Published online in Wiley InterScience (www.interscience.wiley.
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.
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).
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
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.
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).
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
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.
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.
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loss, ancestral, monkey, old, acquisition, macaca, independence, maxillary, world, sinus
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