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Enigmatic Diversity of the Maxillary Sinus in Macaques and Its Possible Role as a Spatial Compromise in Craniofacial Modifications

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Abstract

Understanding the evolutionary significance of morphological diversity is a major goal of evolutionary biology. Paranasal sinuses, which are pneumatized hollow spaces in the face, have attracted attention from researchers as one of the most intriguing traits that show unexpected variations. Macaques are one genus of primates that have accomplished adaptive radiation and therefore present an excellent opportunity to investigate the phenotypic diversification process. Using the large data set of computed tomography images of macaques (172 specimens from 17 species), we applied geometric morphometrics and multivariate analyses to quantitatively evaluate the maxillary sinus (one of the largest paranasal sinuses), the outer craniofacial shape, and nasal cavity. We then applied phylogenetic comparative methods to test their morphological interactions, phylogenetic, and ecogeographical significances. The results showed that the relative maxillary sinus size was significantly associated with the relative nasal cavity size and with the zygomaxillary surface shape. The relative nasal cavity size had ecogeographical correlations and high phylogenetic signal, whereas the zygomaxillary surface shapes were ecogeographically and phylogenetically irrelevant. The significant interactions with multiple surrounding traits that have experienced different evolutionary processes probably enable the maxillary sinus to show enigmatic diversity, which is independent of phylogeny and ecology. The pliable nature of the maxillary sinus, which is positioned between the nasal airways and the outer face, may play a role as a spatial compromise in craniofacial modifications.

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References

  • Adams, D. C., & Otárola Castillo, E. (2013). Geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4(4), 393–399.

    Article  Google Scholar 

  • Albrecht, G. H. (1978). The craniofacial morphology of the Sulawesi macaques: Multivariate approaches to biological problems. Contributions to primatology, 13, 1–151.

    Google Scholar 

  • Allen, W. L., Stevens, M., & Higham, J. P. (2014). Character displacement of Cercopithecini primate visual signals. Nature Communications, 5, 4266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews, P., & Martin, L. (1987). Cladistic relationships of extant and fossil hominoids. Journal of Human Evolution, 16(1), 101–118.

    Article  Google Scholar 

  • Antón, S. C. (1996). Cranial adaptation to a high attrition diet in Japanese macaques. International Journal of Primatology, 17(3), 401–427.

    Article  Google Scholar 

  • Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10 k trees website: A new online resource for primate phylogeny. Evolutionary Anthropology, 19(3), 114–118.

    Article  Google Scholar 

  • Bastir, M., & Rosas, A. (2013). Cranial airways and the integration between the inner and outer facial skeleton in humans. American Journal of Physical Anthropology, 152(2), 287–293.

    PubMed  Google Scholar 

  • Blanton, P. L., & Biggs, N. L. (1969). Eighteen hundred years of controversy: The paranasal sinuses. American Journal of Anatomy, 124(2), 135–147.

    Article  CAS  PubMed  Google Scholar 

  • Blomberg, S. P., Garland, T, Jr, & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57(4), 717–745.

    Article  PubMed  Google Scholar 

  • Brown, W. L., & Wilson, E. O. (1956). Character displacement. Systematic Zoology, 5(2), 49–64.

    Article  Google Scholar 

  • Butaric, L. N. (2015). Differential scaling patterns in maxillary sinus volume and nasal cavity breadth among modern humans. Anatomical Record, 298(10), 1710–1721.

    Article  Google Scholar 

  • Butaric, L. N., McCarthy, R. C., & Broadfield, D. C. (2010). A preliminary 3D computed tomography study of the human maxillary sinus and nasal cavity. American Journal of Physical Anthropology, 143(3), 426–436.

    Article  PubMed  Google Scholar 

  • Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modeling approach for adaptive evolution. The American Naturalist, 164(6), 683–695.

    Article  Google Scholar 

  • Canty, A., & Ripley, B. (2015). Ripley B. boot: Bootstrap R (S-Plus) functions. R package version 1.3-17.

  • Coleman, M. N., & Colbert, M. W. (2007). Technical note: CT thresholding protocols for taking measurements on three dimensional models. American Journal of Physical Anthropology, 133(1), 723–725.

    Article  PubMed  Google Scholar 

  • Curtis, A. A., Lai, G., Wei, F., & Valkenburgh, B. (2015). Repeated loss of frontal sinuses in arctoid carnivorans. Journal of Morphology, 276(1), 22–32.

    Article  PubMed  Google Scholar 

  • Curtis, A. A., & Van Valkenburgh, B. (2014). Beyond the sniffer: Frontal sinuses in Carnivora. Anatomical Record, 297(11), 2047–2064.

    Article  Google Scholar 

  • Delson, E. (1980). Fossil macaques, phyletic relationships and a scenario of deployment. In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 10–30). New York: Nostrand-Reinhold.

    Google Scholar 

  • Eudey, A. A. (1980). Pleistocene glacial phenomena and the evolution of Asian macaques. In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 52–83). New York: Nostrand Reinhold Ltd.

    Google Scholar 

  • Fa, J. (1989). The genus Macaca: A review of taxonomy and evolution. Mammal Review, 19(2), 45–81.

    Article  Google Scholar 

  • Farke, A. A. (2007). Morphology, constraints, and scaling of frontal sinuses in the hartebeest, Alcelaphus buselaphus (Mammalia: Artiodactyla, Bovidae). Journal of Morphology, 268(3), 243–253.

    Article  PubMed  Google Scholar 

  • Farke, A. A. (2010). Evolution and functional morphology of the frontal sinuses in Bovidae (Mammalia: Artiodactyla), and implications for the evolution of cranial pneumaticity. Zoological Journal of the Linnean Society, 159(4), 988–1014.

    Article  Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125(1), 1–15.

    Article  Google Scholar 

  • Fleagle, J. G. (2013). Primate adaptation and evolution (3rd ed.). San Diego: Academic Press.

    Google Scholar 

  • Fooden, J. (1969). Taxonomy and evolution of the monkeys of Celebes. Bibliotheca Primatologica, 10, 1–148.

    Google Scholar 

  • Fooden, J. (1980). Classification and distribution of living macaques (Macaca Lacépède, 1799). In D. G. Lindburg (Ed.), The Macaques: Studies in ecology, behavior and evolution (pp. 1–9). New York: Van Nostrand Reinhold.

    Google Scholar 

  • Fooden, J. (1982). Ecogeographic segregation of macaque species. Primates, 23(4), 574–579.

    Article  Google Scholar 

  • Fooden, J. (1990). The bear macaques, Macaca arctoides: A systematic review. Journal of Human Evolution, 19, 607–686.

    Article  Google Scholar 

  • Fooden, J. (2000). Systematic review of the rhesus macaques, Macaca mulatta (Zimmermann 1780). Fieldiana Zoology, 96(30), 1–180.

    Google Scholar 

  • Gebo, D. L., MacLatchy, L., Kityo, R., Deino, A., Kingston, J., & Pilbeam, D. (1997). A hominoid genus from the early Miocene of Uganda. Science, 276(5311), 401–404.

    Article  CAS  PubMed  Google Scholar 

  • Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Harmon, L. J., Losos, J. B., Jonathan Davies, T., Gillespie, R. G., Gittleman, J. L., Bryan Jennings, W., et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64(8), 2385–2396.

    PubMed  Google Scholar 

  • Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics, 24(1), 129–131.

    Article  CAS  PubMed  Google Scholar 

  • Holton, N., Yokley, T., & Butaric, L. (2013). The morphological interaction between the nasal cavity and maxillary sinuses in living humans. Anatomical Record, 296(3), 414–426.

    Article  Google Scholar 

  • Holton, N. E., Yokley, T. R., Franciscus, R. G., et al. (2011). Climatic adaptation and Neandertal facial evolution: A comment on Rae et al. (2011). Journal of Human Evolution, 61(5), 624–627.

    Article  PubMed  Google Scholar 

  • Ito, T., Kawamoto, Y., Hamada, Y., & Nishimura, T. D. (2015a). Maxillary sinus variation in hybrid macaques: implications for the genetic basis of craniofacial pneumatization. Biological Journal of the Linnean Society, 115(2), 333–347.

    Article  Google Scholar 

  • Ito, T., Nishimura, T. D., Ebbestad, J. O. R., & Takai, M. (2014a). Computed tomography examination of the face of Macaca anderssoni (Early Pleistocene, Henan, northern China): implications for the biogeographic history of Asian macaques. Journal of Human Evolution, 72, 64–80.

    Article  PubMed  Google Scholar 

  • Ito, T., Nishimura, T. D., Hamada, Y., & Takai, M. (2015b). Contribution of the maxillary sinus to the modularity and variability of nasal cavity shape in Japanese macaques. Primates, 56(1), 11–19.

    Article  PubMed  Google Scholar 

  • Ito, T., Nishimura, T., & Takai, M. (2014b). Ecogeographical and Phylogenetic effects on craniofacial variation in macaques. American Journal of Physical Anthropology, 154(1), 27–41.

    Article  PubMed  Google Scholar 

  • Jungers, W. L., Falsetti, A. B., & Wall, C. E. (1995). Shape, relative size, and size-adjustments in morphometrics. American Journal of Physical Anthropology, 38(S21), 137–161.

    Article  Google Scholar 

  • Kamilar, J. M., & Cooper, N. (2013). Phylogenetic signal in primate behaviour, ecology and life history. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1618), 20120341.

    Article  Google Scholar 

  • Keir, J. (2009). Why do we have paranasal sinuses? The Journal of Laryngology & Otology, 123(01), 4–8.

    Article  CAS  Google Scholar 

  • Klingenberg, C. R. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.

    Article  PubMed  Google Scholar 

  • Koppe, T., Nagai, H., & Rae, T. C. (1999a). The maxillary sinus in primate paleontology and systematics. In T. Koppe, H. Nagai, & K. W. Alt (Eds.), The paranasal sinuses of higher primates: Development, function, and evolution (pp. 177–189). Berlin: Quintessence.

    Google Scholar 

  • Koppe, T., & Ohkawa, Y. (1999). Pneumatization of the facial skelton in catarrhine primates. In T. Koppe, H. Nagai, & K. W. Alt (Eds.), The paranasal sinuses of higher primates: Development, function, and evolution (pp. 77–119). Berlin: Quintessence.

    Google Scholar 

  • Koppe, T., Rae, T. C., & Swindler, D. R. (1999b). Influence of craniofacial morphology on primate paranasal pneumatization. Annals of Anatomy, 181(1), 77–80.

    Article  CAS  PubMed  Google Scholar 

  • Márquez, S. (2008). The paranasal sinuses: The last frontier in craniofacial biology. Anatomical Record, 291(11), 1350–1361.

    Article  Google Scholar 

  • Márquez, S., & Laitman, J. T. (2008). Climatic effects on the nasal complex: A CT imaging, comparative anatomical, and morphometric investigation of Macaca mulatta and Macaca fascicularis. Anatomical Record, 291(11), 1420–1445.

    Article  Google Scholar 

  • Márquez, S., Pagano, A. S., Delson, E., Lawson, W., & Laitman, J. T. (2014). The nasal complex of Neanderthals: An entry portal to their place in human ancestry. Anatomical Record, 297(11), 2121–2137.

    Article  Google Scholar 

  • Mori, F., Hanida, S., Kumahata, K., Miyabe-Nishiwaki, T., Suzuki, J., Matsuzawa, T., et al. (2015). Minor contributions of the maxillary sinus to the air-conditioning performance in macaque monkeys. Journal of Experimental Biology, 218, 2394–2401.

    Article  PubMed  Google Scholar 

  • Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., et al. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3(4), 743–756.

    Article  Google Scholar 

  • Neeser, R., Ackermann, R. R., & Gain, J. (2009). Comparing the accuracy and precision of three techniques used for estimating missing landmarks when reconstructing fossil hominin crania. American Journal of Physical Anthropology, 140(1), 1–18.

    Article  PubMed  Google Scholar 

  • Nishimura, T. D., & Ito, T. (2014). Aplasia of the maxillary sinus in a Tibetan macaque (Macaca thibetana) with implications for its evolutionary loss and reacquisition. Primates, 55(4), 501–508.

    Article  PubMed  Google Scholar 

  • Nishimura, T. D., Ito, T., Yano, W., Ebbestad, J. O. R., & Takai, M. (2014). Nasal architecture in Procynocephalus wimani (Early Pleistocene, China) and implications for its phyletic relationship with Paradolichopithecus. Anthropological Science, 122(2), 101–113.

    Article  Google Scholar 

  • Nishimura, T. D., Senut, B., Prieur, A., Treil, J., & Takai, M. (2009). Nasal architecture of Paradolichopithecus arvernensis (late Pliocene, Seneze, France) and its phyletic implications. Journal of Human Evolution, 56, 213–217.

    Article  PubMed  Google Scholar 

  • Nishimura, T. D., Takai, M., & Maschenko, E. N. (2007). The maxillary sinus of Paradolichopithecus sushkini (late Pliocene, southern Tajikistan) and its phyletic implications. Journal of Human Evolution, 52(6), 637–646.

    Article  PubMed  Google Scholar 

  • Nishimura, T. D., Takai, M., Tsubamoto, T., Egi, N., & Shigehara, N. (2005). Variation in maxillary sinus anatomy among platyrrhine monkeys. Journal of Human Evolution, 49(3), 370–389.

    Article  PubMed  Google Scholar 

  • Noback, M. L., Harvati, K., & Spoor, F. (2011). Climate-related variation of the human nasal cavity. American Journal of Physical Anthropology, 145(4), 599–614.

    Article  PubMed  Google Scholar 

  • O’Higgins, P., Bastir, M., & Kupczik, K. (2006). Shaping the human face. International Congress Series, 1296, 55–73.

    Article  Google Scholar 

  • Orme, D., Franckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., et al. (2013). Caper: Comparative analyses of phylogenetics and evolution in R. R package version 0.5.2.

  • Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401(6756), 877–884.

    Article  CAS  PubMed  Google Scholar 

  • Pan, R., & Oxnard, C. E. (2002). Craniodental variation among Macaques (Macaca), nonhuman primates. BMC Evolutionary Biology, 2, 1–12.

    Article  Google Scholar 

  • Pennell, M. W., & Harmon, L. J. (2013). An integrative view of phylogenetic comparative methods: Connections to population genetics, community ecology, and paleobiology. Annals of the New York Academy of Sciences, 1289(1), 90–105.

    Article  PubMed  Google Scholar 

  • Pérez de los Ríos, M., Moyà-Solà, S., & Alba, D. M. (2012). The nasal and paranasal architecture of the Middle Miocene ape Pierolapithecus catalaunicus (Primates: Hominidae): Phylogenetic implications. Journal of Human Evolution, 63(3), 497–506.

    Article  PubMed  Google Scholar 

  • Polly, P. D., Lawing, A. M., Fabre, A.-C., & Goswami, A. (2013). Phylogenetic principal components analysis and geometric morphometrics. Hystrix, the Italian Journal of Mammalogy, 24(1), 33–41.

    Google Scholar 

  • Racicot, R. A., & Berta, A. (2013). Comparative morphology of porpoise (Cetacea: Phocoenidae) pterygoid sinuses: Phylogenetic and functional implications. Journal of Morphology, 274(1), 49–62.

    Article  PubMed  Google Scholar 

  • Rae, T. C. (2008). Paranasal pneumatization in extant and fossil Cercopithecoidea. Journal of Human Evolution, 54(3), 279–286.

    Article  PubMed  Google Scholar 

  • Rae, T. C., Hill, R. A., Hamada, Y., & Koppe, T. (2003). Clinical variation of sinus volume in Japanese macaques (Macaca fuscata). American Journal of Primatology, 59(4), 153–158.

    Article  PubMed  Google Scholar 

  • Rae, T. C., & Koppe, T. (2000). Isometric scaling of maxillary sinus volume in hominoids. Journal of Human Evolution, 38(3), 411–423.

    Article  CAS  PubMed  Google Scholar 

  • Rae, T. C., & Koppe, T. (2004). Holes in the head: Evolutionary interpretations of the paranasal sinuses in catarrhines. Evolutionary Anthropology, 13(6), 211–223.

    Article  Google Scholar 

  • Rae, T. C., & Koppe, T. (2008). Independence of biomechanical forces and craniofacial pneumatization in Cebus. Anatomical Record, 291(11), 1414–1419.

    Article  Google Scholar 

  • Rae, T. C., & Koppe, T. (2014). Sinuses and flotation: Does the aquatic ape theory hold water? Evolutionary Anthropology, 23(2), 60–64.

    Article  PubMed  Google Scholar 

  • Rae, T. C., Koppe, T., & Nagai, H. (1997). Maxillary sinus reduction due to cold stress in the Macaca fascisularis species group. American Journal of Physical Anthropology, Suppliment, 24, 190–191.

    Google Scholar 

  • Rae, T. C., Koppe, T., Spoor, F., Benefit, B., & McCrossin, M. (2002). Ancestral loss of the maxillary sinus in old world monkeys and independent acquisition in Macaca. American Journal of Physical Anthropology, 117(4), 293–296.

    Article  PubMed  Google Scholar 

  • Rae, T. C., Koppe, T., & Stringer, C. B. (2011a). The Neanderthal face is not cold adapted. Journal of Human Evolution, 60(2), 234–239.

    Article  PubMed  Google Scholar 

  • Rae, T. C., Koppe, T., Stringer, C. B., et al. (2011b). Hyperpneumatized Neanderthals? Reply to Holton et al. (2011). Journal of Human Evolution, 61(5), 628–629.

    Article  Google Scholar 

  • Rae, T. C., Vidarsdottir, U. S., Jeffery, N., & Steegmann, A. T. (2006). Developmental response to cold stress in cranial morphology of Rattus: implications for the interpretation of climatic adaptation in fossil hominins. Proceedings of the Royal Society B: Biological Sciences, 273(1601), 2605–2610.

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team. 2015. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • Revell, L. J. (2009). Size correction and principal components for interspecific comparative studies. Evolution, 63(12), 3258–3268.

    Article  PubMed  Google Scholar 

  • Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223.

    Article  Google Scholar 

  • Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55(11), 2143–2160.

    Article  CAS  PubMed  Google Scholar 

  • Rossie, J. B. (2008). The phylogenetic significance of anthropoid paranasal sinuses. Anatomical Record, 291(11), 1485–1498.

    Article  Google Scholar 

  • Rossie, J. B., Simons, E. L., Gauld, S. C., & Rasmussen, D. T. (2002). Paranasal sinus anatomy of Aegyptopithecus: implications for hominoid origins. Proceedings of the National Academy of Sciences of the United States of America, 99(2), 8454–8456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santana, S. E., Alfaro, J. L., & Alfaro, M. E. (2012). Adaptive evolution of facial colour patterns in Neotropical primates. Proceedings of the Royal Society B: Biological Sciences, 279(1736), 2204–2211.

    Article  PubMed  PubMed Central  Google Scholar 

  • Santana, S. E., Alfaro, J. L., Noonan, A., & Alfaro, M. E. (2013). Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines. Nature Communications, 4, 2765.

    Article  PubMed  Google Scholar 

  • Santana, S. E., Dobson, S. D., & Diogo, R. (2014). Plain faces are more expressive: Comparative study of facial colour, mobility and musculature in primates. Biology Letters, 10(5), 20140275.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schlager, S. (2015). Morpho: Calculations and visualisations related to Geometric Morphometrics. R package version 2.3.0.

  • Shea, B. T. (1977). Eskimo craniofacial morphology, cold stress and the maxillary sinus. American Journal of Physical Anthropology, 47(2), 289–300.

    Article  CAS  PubMed  Google Scholar 

  • Smith, R. J. (1984). Determination of relative size: The “criterion of subtraction” problem in allometry. Journal of Theoretical Biology, 108(1), 131–142.

    Article  CAS  PubMed  Google Scholar 

  • Smith, T. D., Rossie, J. B., Cooper, G. M., Carmody, K. A., Schmieg, R. M., Bonar, C. J., et al. (2010). The maxillary sinus in three genera of new world monkeys: Factors that constrain secondary pneumatization. Anatomical Record, 293(1), 91–107.

    Article  Google Scholar 

  • Smith, T. D., Rossie, J. B., Cooper, G. M., Schmieg, R. M., Bonar, C. J., Mooney, M. P., et al. (2011). Comparative microcomputed tomography and histological study of maxillary pneumatization in four species of new world monkeys: the perinatal period. American Journal of Physical Anthropology, 144(3), 392–410.

    Article  PubMed  Google Scholar 

  • Takahashi, L. K., & Pan, R. (1994). Mandibular morphometrics among macaques: The case of Macaca thibetana. International Journal of Primatology, 15(4), 597–621.

    Article  Google Scholar 

  • Takai, M., Maschenko, E. N., Nishimura, T. D., Anezaki, T., & Suzuki, T. (2008). Phylogenetic relationships and biogeographic history of Paradolichopithecus suskini Trofimov 1977, a large-bodied cercopithecus monkey from the Pliocene of Eurasia. Quaternary International, 179(1), 108–119.

    Article  Google Scholar 

  • Warton, D. I., Duursma, R. A., Falster, D. S., & Taskinen, S. (2012). Smatr 3–an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3(2), 257–259.

    Article  Google Scholar 

  • Witmer, L. M. (1997). The evolution of the antorbital cavity of Archosaurs: A study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Journal of Vertebrate Paleontology, 17(1), 1–73.

    Article  Google Scholar 

  • Witmer, L. M. (1999). The phylogenetic history of the paranasal air sinuses. In T. Koppe, H. Nagai, & K. W. Alt (Eds.), The paranasal sinuses of higher primates (pp. 21–34). Berlin: Quintessence.

    Google Scholar 

  • Witmer, L. M., & Ridgely, R. C. (2008). The paranasal air sinuses of predatory and armored dinosaurs (Archosauria: Theropoda and Ankylosauria) and their contribution to cephalic structure. Anatomical Record, 291(11), 1362–1388.

    Article  Google Scholar 

  • Yokley, T. R. (2009). Ecogeographic variation in human nasal passages. American Journal of Physical Anthropology, 138(1), 11–22.

    Article  PubMed  Google Scholar 

  • Zollikofer, C. P. E., De Leon, M. S. P., Schmitz, R. W., & Stringer, C. B. (2008). New insights into Mid-Late Pleistocene fossil hominin paranasal sinus morphology. Anatomical Record, 291(11), 1506–1516.

    Article  Google Scholar 

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Acknowledgments

We thank D. Shimizu, T. Takano, Y. Shintaku, H. Taru, H. Hirotani, H. Takahashi, and N. Shigehara for kindly providing access to the specimens; and S. Kondo, N. Ogihara, M. Nakatsukasa, W. Yano, Thaung Htike, and Zin-Maung-Maung-Thein for their help with CT scanning. We also thank B. Hallgrimsson, C. Rolian, and two anonymous reviewers for their constructive comments that significantly improved our manuscript. This study was funded by JSPS Grants-in-Aid for Scientific Research (Grant 26650171 to T.D.N.; Grant 26304019 to M. Takai).

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  1. Department of Human Biology and Anatomy, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, 903-0215, Japan

    Tsuyoshi Ito

  2. Japan Society for the Promotion of Science, Tokyo, Japan

    Tsuyoshi Ito

  3. Department of Evolution and Phylogeny, Primate Research Institute, Kyoto University, Inuyama, Aichi, 484-8506, Japan

    Takeshi D. Nishimura

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Ito, T., Nishimura, T.D. Enigmatic Diversity of the Maxillary Sinus in Macaques and Its Possible Role as a Spatial Compromise in Craniofacial Modifications. Evol Biol 43, 414–426 (2016). https://doi.org/10.1007/s11692-016-9369-4

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