Phylogenetic relationship of a fossil macaque (Macaca cf. robusta) from the Korean Peninsula to extant species of macaques based on zygomaxillary morphology.

Little is known about the biogeographical and evolutionary histories of macaques (Macaca spp.) in East Asia because the phylogenetic positions of fossil species remain unclear. Here we examined the zygomaxillary remains of a fossil macaque (M. cf. robusta) from the Durubong Cave Complex, South Korea, that dates back to the late Middle to Late Pleistocene, to infer its phylogenetic relationship to extant species. We took 195 fixed- and semi-landmarks from the zygomaxillary regions of the fossil specimen and from 147 specimens belonging to 14 extant species. We then conducted a generalized Procrustes analysis followed by a multivariate statistical analysis to evaluate the phenetic affinities of the fossil to the extant species and reconstructed the most parsimonious phylogenetic tree using a phylogenetic morphometric approach. We found that the fossil was most similar to Macaca fuscata (Japanese macaque) in the zygomaxillary morphospace although it was at the limit of the range of variation for this species. The second closest in the morphospace was the continental Macaca mulatta (rhesus macaque). Parsimonious reconstruction confirmed that the fossil was most closely related to M. fuscata, even after controlling for the effects of allometry. These findings suggest that in the late Middle to Late Pleistocene, close relatives of M. fuscata that looked like the extant species were distributed on the Korean Peninsula, where no species of macaques are found today. Thus, some morphological characteristics of M. fuscata may have developed before its ancestor dispersed into the Japanese archipelago.

First discovery of colobine fossils from the Late Miocene/Early Pliocene in central Myanmar.

Here we report two kinds of colobine fossils discovered from the latest Miocene/Early Pliocene Irrawaddy sediments of the Chaingzauk area, central Myanmar. A left mandibular corpus fragment preserving M1-3 is named as a new genus and species, Myanmarcolobus yawensis. Isolated upper (M(1)?) and lower (M2) molars are tentatively identified as Colobinae gen. et sp. indet. Although both forms are medium-sized colobines, they are quite different from each other in M2 morphology. The isolated teeth of the latter show typical colobine-type features, so it is difficult to identify their taxonomic position, whereas lower molars of Myanmarcolobus have unique features, such as a trapezoid-shaped long median lingual notch, a deeply concave median buccal cleft, a strongly developed mesiobuccal notch, and rather obliquely running transverse lophids. Compared with fossil and living Eurasian colobine genera, Myanmarcolobus is most similar in lower molar morphology to the Pliocene Dolichopithecus of Europe rather than to any Asian forms. In Dolichopithecus, however, the tooth size is much larger and the median lingual notch is mesiodistally much shorter than that of Myanmarcolobus. The discovery of Myanmarcolobus in central Myanmar is the oldest fossil record in Southeast Asia not only of colobine but also of cercopithecid monkeys and raises many questions regarding the evolutionary history of Asian colobine monkeys.

Minor contributions of the maxillary sinus to the air-conditioning performance in macaque monkeys.

The nasal passages mainly adjust the temperature and humidity of inhaled air to reach the alveolar condition required in the lungs. By contrast to most other non-human primates, macaque monkeys are distributed widely among tropical, temperate and subarctic regions, and thus some species need to condition the inhaled air in cool and dry ambient atmospheric areas. The internal nasal anatomy is believed to have undergone adaptive modifications to improve the air-conditioning performance. Furthermore, the maxillary sinus (MS), an accessory hollow communicating with the nasal cavity, is found in macaques, whereas it is absent in most other extant Old World monkeys, including savanna monkeys. In this study, we used computational fluid dynamics simulations to simulate the airflow and heat and water exchange over the mucosal surface in the nasal passage. Using the topology models of the nasal cavity with and without the MS, we demonstrated that the MS makes little contribution to the airflow pattern and the air-conditioning performance within the nasal cavity in macaques. Instead, the inhaled air is conditioned well in the anterior portion of the nasal cavity before reaching the MS in both macaques and savanna monkeys. These findings suggest that the evolutionary modifications and coetaneous variations in the nasal anatomy are rather independent of transitions and variations in the climate and atmospheric environment found in the habitats of macaques.

Computed tomography examination of the face of Macaca anderssoni (Early Pleistocene, Henan, northern China): Implications for the biogeographic history of Asian macaques.

Macaca anderssoni, a fossil macaque from the Early Pleistocene of northern China, has attracted much attention from researchers in terms of reconstructing the biogeographic history of Asian macaques, while its phylogenetic position remains debatable. In the present study, we evaluated patterns of variation in external and internal craniofacial morphologies among four phylogenetic groups of extant macaques (the fascicularis, sinica, silenus, and sylvanus groups), using computed tomography and multivariate analyses. We also reassessed the holotype of M. anderssoni, a partial cranium preserving the face and palate, to evaluate the phylogenetic group to which M. anderssoni is most closely related. Facial elongation was found to be significantly influenced by size. The particular combination of some allometric and non-allometric shape components was found to reflect phylogenetic relationships; however, these features of M. anderssoni fall intermediate among the four phylogenetic groups, with no typical similarities to any one group. The variations in nasal cavity shape were found to reflect phylogenetic relationships but those of the maxillary sinus did not. Macaca anderssoni has a nasal cavity that is laterally expanded anteriorly and constricted posteriorly, a unique morphology among macaques and shared only with larger members of the sinica group. This unique feature is considered to be a derived condition among macaques, suggesting that M. anderssoni is phylogenetically related to the sinica group (especially M. assamensis, M. thibetana, and M. arctoides) and that the populations of the sinica group were distributed in northern China during the Early Pleistocene. Currently, the populations of the sinica group are not distributed in northern East Asia, while those of the fascicularis group are. Thus, probably due to climatic deterioration in the Late Pleistocene, the former lineage has retreated southward or has become extinct in this region, being replaced by the latter lineage.

Reassessment of Dolichopithecus (Kanagawapithecus) leptopostorbitalis, a colobine monkey from the Late Pliocene of Japan.

In the original description of Dolichopithecus (Kanagawapithecus) leptopostorbitalis, Iwamoto, Hasegawa and Koizumi, 2005, a moderately large-sized colobine monkey from the Late Pliocene of central Japan, affinities to the European Dolichopithecus rather than to the Transbaikalian Parapresbytis were noted based on the similarities in cranial morphology. Computed tomography scans confirm the presence of the maxillary sinus in the holotype, whereas it is probably absent in specimens of the European Dolichopithecus ruscinensis, the type species of this genus. This feature is either present or absent homogeneously in any given genus of living anthropoids. Its presence or absence is unknown in Parapresbytis, but the distinct morphology of the maxillary incisors in this taxon suggests that this form had different feeding habits from the Japanese colobines. These findings suggest that the Japanese colobine should be referred to henceforth as Kanagawapithecus leptopostorbitalis. Kanagawapithecus shares many important facial and dental features with Dolichopithecus rather than with Parapresbytis, but this association depends largely on the limited availability of comparable materials for the latter. Among colobines, the presence of the maxillary sinus is recorded only in Libypithecus and Cercopithecoides. The maxillary sinus is absent in all modern Asian colobines, implying that Kanagawapithecus is an isolated form without any relationship to living forms. Nevertheless, such phylogenetic interpretations are largely dependent on the restricted fossil evidence from the Pliocene and Pleistocene of eastern Eurasia and will be reexamined when new findings are made.

Nasal anatomy of Paradolichopithecus gansuensis (early Pleistocene, Longdan, China) with comments on phyletic relationships among the species of this genus.

Paradolichopithecus was a large cercopithecine primate that existed in Eurasia from the middle Pliocene to the early Pleistocene. Para. arvernensis from the late Pliocene of Senèze, France, shows no maxillary sinus, whereas Para.sushkini from the late Pliocene of Kuruksay, Tajikistan, has this feature. In this study, we examined a new maxillary specimen of Para. gansuensis from the early Pleistocene of Longdan, China. The Longdan maxilla had lost its facial part, which exposed the internal floor of the nasal region. The nasal floor expands laterally, making the maxillary body thin at the P3-M2 level and thick at the M3 level and extending to the maxillary tubercle. Such a topography is seen in the Senèze and Kuruksay crania. The Longdan maxilla shows no evidence of the formation of a maxillary sinus within the inferior portion of the thick maxillary body, as is seen in the Senèze cranium. Such a configuration could reflect the absence of a maxillary sinus in the Longdan specimen. Eastern Para. gansuensis might have dispersed eastward retaining a primitive condition, while central Para. sushkini would have acquired this feature independently in central Eurasia.

Contribution of the maxillary sinus to the modularity and variability of nasal cavity shape in Japanese macaques.

The nasal cavity is essential for conditioning of inspired air, and its form likely impacts its function. Since humans and other anthropoids have reduced nasal turbinates when compared to other mammals, variation in relative surface area is mainly brought about by changes to overall nasal architecture. Previous studies of modern humans suggest that variation in the transverse dimensions of the nasal cavity is likely possible because of the presence of the maxillary sinuses. To understand the evolutionary origin of this adaptation, we investigated the nasofacial skeleton of Japanese macaques (Macaca fuscata). We applied computed tomography and geometric morphometrics to test how the nasal cavity shape is correlated with relative maxillary sinus volume and to evaluate how the nasal cavity shape is integrated with the external craniofacial shape. Our results show that the decreasing sinus volume is well associated with the relative expansion of nasal cavity at the middle region compared to the anterior and posterior openings. The nasal cavity shape is not integrated with the external craniofacial shape especially at the middle region as well as the posterior opening. Thus, the maxillary sinus in macaques may contribute to the modularity and variability of the nasal cavity shape, possibly facilitating the adaptive changes in the nasal airways of this species.

Aplasia of the maxillary sinus in a Tibetan macaque (Macaca thibetana) with implications for its evolutionary loss and reacquisition.

The skull of an adult female Tibetan macaque, Macaca thibetana, was found to completely lack the maxillary sinus (MS). This absence was accompanied by a slight lateral concavity where the ostium should have formed in the MS, a slight drop of the orbital floor, posterior and medial displacement of the zygomaxillary suture, an unusual position of the lacrimal canal, malocclusion with severely worn cheek teeth, and abnormalities in the temporomandibular joints. The facial component was disproportionally large compared with the neurocranium and mandible. This hypertrophic face probably caused the malocclusion and associated anatomical disorders and simultaneously displaced the lacrimal canal posterior to other nasal structures to preclude the possibility of maxillary pneumatization. These modifications in the spatial relationships to nasal structures might help explain the evolutionary loss and reacquisition of the MS in some primate lineages displaying great variations in facial anatomy.

The maxillary sinus of Paradolichopithecus sushkini (late Pliocene, southern Tajikistan) and its phyletic implications.

Paradolichopithecus sushkini is a large fossil cercopithecine from the late Pliocene discovered at Kuruk-Say, southern Tajikistan. Despite its rather long face and large size, many authorities regard Paradolichopithecus not as a baboon, but as a large macaque, mainly based on the cranial morphology of European specimens. Among Old World monkeys, macaques are the only species that possess a maxillary sinus. Thus, we evaluated the presence/absence and morphology of this feature in P. sushkini using computed tomography (CT) scans of two Kuruk-Say cranial specimens in order to assess this species' taxonomic affinities. One of the specimens shows a thin bony wall separating a small area from the nasal cavity. Posterior to this structure is a pair of bony ridges: one protrudes from the alveolar process and the other descends from the superior portion of the nasal wall. A similar configuration was detected in the other specimen. These features strongly suggest the presence of a maxillary sinus in this species. This interpretation is supported by the fact that the superior portion of the alveolar process is excavated in the adult specimen. Thus, both specimens exhibit a maxillary sinus expanding laterally to share the external thin wall of the muzzle, and such a configuration may depend on the reduction of the maxillary bone, i.e., the presence of a maxillary fossa. The Kuruk-Say specimens probably retained a small maxillary sinus, despite the reduced size of the maxillary body. Thus, based on this evidence, P. sushkini probably belongs to the macaque lineage rather than that of baboons, although structural influences of the maxillary fossa leading to formation of the maxillary sinus have yet to be evaluated in extant macaques and baboons.

Variation in maxillary sinus anatomy among platyrrhine monkeys.

Variations in the maxillary sinus anatomy of extant and fossil catarrhine primates have been extensively examined using computed tomography (CT), and have potential utility for phylogenetic analyses. This approach has also been used to demonstrate its anatomical variation in eight of the 16 extant genera of platyrrhines and the absence of the sinus in Saimiri and Cacajao. We used this approach to evaluate the three-dimensional anatomy of the maxillary sinus in all extant platyrrhine genera, and here argue the phylogenic implications of this variation. This study confirms, for the most part, previous CT studies and augments them with the six genera not studied previously: Ateles, Lagothrix, Callithrix, Cebuella, Pithecia and Chiropotes. The entire maxilla is pneumatized by the sinus in the atelines, Cebus, and Callicebus, whereas the sinus pneumatizes only the medial part of the maxilla in the callitrichines and Aotus. Pithecia has a unique conformation in which the maxillary sinus and the expanded inferior meatus pneumatize the posteromedial and anterolateral parts of the entire maxilla, respectively. Chiropotes has no sinus, and the inferior meatus possibly expands into the area between the middle meatus and medial surface of the maxilla to disturb sinus formation, as in the case of its close relative Cacajao. Finally, we argue that the sinus that pneumatizes the entire maxilla is a primitive feature in extant platyrrhines and was probably shared by the last common ancestor of the anthropoids.