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Lufengpithecus Is Known from a Number of Late Although YV0999 Was Recovered in 1988 (18) and Has Been the Miocene Sites in Yunnan Province in Southern China

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Lufengpithecus Is Known from a Number of Late Although YV0999 Was Recovered in 1988 (18) and Has Been the Miocene Sites in Yunnan Province in Southern China Juvenile hominoid cranium from the late Miocene of southern China and hominoid diversity in Asia Jay Kelleya,1 and Feng Gaob aInstitute of Human Origins and School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287; and bDepartment of Paleoanthropology, Yunnan Institute of Cultural Relics and Archaeology, Kunming, Yunnan 650118, China Edited by Erik Trinkaus, Washington University, St. Louis, MO, and approved March 23, 2012 (received for review January 24, 2012) The fossil ape Lufengpithecus is known from a number of late Although YV0999 was recovered in 1988 (18) and has been the Miocene sites in Yunnan Province in southern China. Along with subject of a preliminary analysis (20), it has not been analyzed other fossil apes from South and Southeast Asia, it is widely con- within an adequate comparative framework of similarly aged sidered to be a relative of the extant orangutan, Pongo pygmaeus. juveniles of extant great apes. Therefore, a database was assem- It is best represented at the type site of Shihuiba (Lufeng) by bled of measurements and discrete, nonmetric characters from several partial to nearly complete but badly crushed adult crania. extant great ape individuals, representing Gorilla gorilla, Pan There is, however, an additional, minimally distorted cranium of a troglodytes and Pongo pygmaeus (each species sample comprising young juvenile from a nearly contemporaneous site in the Yuan- a single subspecies), at approximately the same stage of dental mou Basin, which affords the opportunity to better assess the rela- development as YV0999. The measurements reflect general shape tionships between Lufengpithecus and Pongo. Comparison with and proportional relationships of the facial skeleton and were similarly aged juvenile skulls of extant great apes reveals no fea- evaluated using both cluster analysis and discriminant analysis tures suggesting clear affinities to orangutans, and instead reveals (Materials and Methods and SI Text) to determine the overall a morphological pattern largely consistent with a stem member of phenetic resemblance of YV0999 with respect to the extant great the hominid (great ape and human) clade. The existence at this ape crania. The nonmetric characters reflect consensus or near time of other hominids in South Asia (Sivapithecus) and Southeast consensus cranial apomorphies of each of the extant great apes fi Asia (Khoratpithecus) with clear craniofacial af nities to Pongo (21) that were found to be at least incipiently expressed at a stage suggests both more diversity among Asian Late Miocene apes of development equivalent to that of YV0999. YV0999 was scored and more complex patterns of dispersal than previously supposed. for these characters, which were evaluated individually rather Major differences in the associated mammal faunas from the south- than by formal, computational cladistic analysis. ern China sites and those from South and Southeast Asia are con- sistent with these findings and suggest more than one dispersal Results route of apes into East Asia earlier in the Miocene. Results of the cluster analysis are shown in Fig. 2. YV0999 groups as an outlier to the majority of the Pan crania. Interestingly, Pan he hominoid Lufengpithecus from the late Miocene of clusters with Pongo rather than with its sister taxon, Gorilla, Tsouthern China is known mostly from hundreds of isolated highlighting the distinctiveness of the proportions and overall teeth, principally from the sites of Shihuiba (Lufengpithecus shape of the gorilla facial skeleton at this stage of development. lufengensis; ca. 6–7 Ma) (1, 2) and several somewhat older sites in Although most of the great ape crania group with their con- the Yuanmou Basin (Lufengpithecus hudienensis; ca. 7–8 Ma) (2– specifics, there is a fourth, taxonomically heterogeneous cluster 4). The molar teeth are strikingly similar to the highly distinctive that includes crania of all three taxa, but primarily Pongo, and that teeth of the modern orangutan, with intricately wrinkled enamel is linked to the Pan plus Pongo cluster (Fig. 2). This cluster reveals over relatively flattened occlusal basins. There are also several that possession by some individuals of certain metric character- badly crushed crania from Shihuiba (5–7). Restoration has been istics that are more typical of one of the other genera was enough attempted for one of these (8), but some of the morphology to create a separate grouping of these somewhat anomalous remains ambiguous or is clearly still distorted. The condition of individuals. It also highlights the fact that, although the juvenile fi these crania has allowed for different interpretations of their crania of each genus largely express their genus-speci c metric morphology and, consequently, different opinions regarding the characteristics, there is greater similarity in the shape of the facial phylogenetic position of Lufengpithecus (4, 8–11). Nevertheless, skeleton among the three great ape genera at the early juvenile stage than as adults. most recent analyses propose a relationship to the Pongo clade, fi as either its nearest relative or as a stem member of the clade The discriminant analysis was more de nitive. The results are – highly significant (Wilk’s lambda P value, <0.001), and all 30 (12 17). fi The cranium of L. hudienensis from Yuanmou, YV0999, pre- extant great ape crania were correctly classi ed. YV0999 was entered as an unknown and did not, therefore, contribute to the serves nearly the entire facial skeleton, the palate with partial computation. Among the three extant great ape group means, dentition, and most of the frontal bone. In contrast to the Shihuiba YV0999 is closest to Pan (Mahalanobis D2 values to the group crania, it is remarkably well preserved and minimally distorted, means of, respectively, Pan, Gorilla, and Pongo: 73.26, 119.13, with the right side being almost completely free of distortion (Fig. and 155.64), and in a forced classification, it was grouped with 1, Fig. S1,andSI Text) (18, 19). Because of its preservation, this Pan (P > 0.999). cranium can be more informative about the phylogenetic rela- tionships of Lufengpithecus than are the damaged adult crania fi from Shihuiba. However, its juvenile status ( rst molar just coming Author contributions: J.K. designed research; J.K. performed research; J.K. and F.G. ana- into occlusion) introduces an additional challenge for interpre- lyzed data; and J.K. wrote the paper. tation because there are no other relatively complete juvenile The authors declare no conflict of interest. crania, and even few juvenile cranial fragments, known for other This article is a PNAS Direct Submission. Miocene anthropoids. Additionally, little has been done to identify 1To whom correspondence should be addressed. E-mail: [email protected]. the developmental stages at which the derived features (apomor- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. phies) characteristic of adult great ape crania first become evident. 1073/pnas.1201330109/-/DCSupplemental. 6882–6885 | PNAS | May 1, 2012 | vol. 109 | no. 18 www.pnas.org/cgi/doi/10.1073/pnas.1201330109 Downloaded by guest on September 28, 2021 S2), minimal offset from the nasoalveolar clivus to the palate in- tranasally with a highly constricted incisive canal, a continuously concave midfacial profile, and lack of a frontal sinus (21, 22). In these, YV0999 is decidedly unlike Pongo and more closely resem- bles Pan and Gorilla, especially the former, which both express variants of the ancestral hominid condition for these features (21). In most features of facial morphology, YV0999 most closely resembles Pan, arguably the least derived of the extant great apes in terms of cranial morphology. The principal differences are in the relatively large orbits of YV0999 and their influence on widening the upper face and the absence of the most clearly de- rived features of Pan, a supraorbital torus and sulcus and a sharply posteriorly inflected malar region. YV0999 also has a shorter, flatter, and more steeply inclined premaxilla, a premaxillary su- ture that is completely fused over its entire extent (in none of the extant ape crania is this suture completely fused at this stage of development, and it is mostly fused in only five of the 30 indi- viduals in the sample), and two distinct, large incisive foramina palatally, indicating a fully partitioned incisive canal. The incisive Fig. 1. Oblique frontal view (Left) and lateral view (Right) of YV0999, canal is at most only partly partitioned at this stage of de- Lufengpithecus hudienensis. Note the missing bone at the inferior nasal velopment in the African ape crania, whereas it is unpartitioned in margin in the frontal view. In the lateral view, the actual facial contour is Pongo and remains so in adulthood. somewhat obscured by the broken and everted left nasal margin, but the slight anterior projection of the inferior nasal bones, resulting in a biconcave Discussion facial profile, is nonetheless evident. (Scale bar: 1 cm.) Assuming that YV0999 is representative of cranial morphology in other Lufengpithecus species (SI Text), we consider it most Despite the small, taxonomically heterogeneous group in the probable that Lufengpithecus represents a stem hominid lineage cluster analysis, the results from the cluster and discriminant that also expresses a small suite of uniquely derived features (4, analyses together affirm the distinctiveness of facial form among 9, 23). It is also possible given the general resemblance
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