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 consistent 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 relationships 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 resembles 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 derived 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 suture 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 individuals 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 to Pan, the three extant great apes at this early stage of development and exclusive of the derived features of extant African apes noted in demonstrate the resemblance of YV0999 to Pan rather than Table 1, that Lufengpithecus represents a stem member of the to Pongo. African ape and human clade (20) (discussed further below). Results of the discrete character analysis are shown in Table 1. Although the absence of Pongo apomorphies in YV0999 does Many of the most distinctive apomorphic features of extant great not absolutely preclude Lufengpithecus being a member of the ape crania are clearly expressed at the developmental stage rep- Pongo clade, these absences take on added significance in light of resented by incipient first molar occlusion. For none of these does the fact that most of the key derived facial skeletal features of ANTHROPOLOGY YV0999 show the presumed derived condition, regardless of the Pongo are expressed in the nearly contemporaneous Sivapithecus extant ape that expresses the particular apomorphy. It instead sivalensis from the late Miocene Siwaliks of South Asia (13, 22), expresses a generally plesiomorphic morphology that would be whereas at least one is expressed in Khoratpithecus piriyai from expected in the common ancestor of the hominid (great ape and the late Miocene site of Khorat in Thailand (24, 25) and K. human) clade. Most important, it shares none of the consensus ayeyarwadyensis from the Irrawaddy Formation in Myanmar (26). derived features of Pongo. Six of these in particular are highly Sivapithecus shares all of the derived features of Pongo listed in distinctive among apes, both fossil and extant: superiorly-inferiorly Table 1. Mandibles of K. piriyai and K. ayeyarwadyensis show no elongate orbits, a relatively very narrow interorbital region (Fig. evidence of attachment of anterior digastric muscles, an absence otherwise recorded only in Pongo among both fossil and extant apes. In addition, the pattern of mandibular postcanine root morphology in both Khoratpithecus species is most similar to that Gorilla Gorilla of Pongo among extant great apes (27). The presence of key de- Gorilla Gorilla rived features of Pongo in these other, contemporary South Asian Gorilla Gorilla genera reinforces the argument that the absence of these features Gorilla Gorilla in Lufengpithecus indicates exclusion from the Pongo clade. Gorilla Pan A phylogenetic link between Sivapithecus and Khoratpithecus Pongo Pongo to the exclusion of Lufengpithecus is also supported by the Pongo Pongo mammalian faunas from the different fossil sites. There are Pan Pan major differences at the family level between the large mammal Pan Pan faunas from southern China on the one hand and those from Pan South (Siwaliks) and Southeast Asia (Khorat, Irrawaddy For- Pan Pan mation) on the other (Table 2). Certain families that are com- Pan Pan mon or dominant elements in the southern China faunas, some Yuanmou Pongo shared with faunas from northern China, are absent from the Pongo Pongo faunas of South and Southeast Asia. Likewise, certain families Pongo Pongo that are common in the South and Southeast Asian faunas are Pongo Pongo absent from those of southern China. There are further differences in the composition of these faunas. Bovids, for example, 0.0 0.1 0.2 0.3 0.4 0.5 are both common and diverse in the South/Southeast Asian Distances faunas but are either rare/absent (Yuanmou) or uncommon and Fig. 2. Cluster tree of extant great ape juvenile crania and YV0999 based on with low diversity (Shihuiba) in the faunas from southern China. craniofacial measurements (Materials and Methods and SI Text). The faunas from South and Southeast Asia also have in common

Kelley and Gao PNAS | May 1, 2012 | vol. 109 | no. 18 | 6883 Downloaded by guest on September 28, 2021 Table 1. Discrete craniofacial features in extant great apes and YV0999 Morphology Derived condition and taxon in which it is expressed YV0999 resembles

Frontal squama orientation More horizontally angled back from supraorbital area (Pan/Gorilla) Pongo Supraorbital topography Torus and sulcus (Pan/Gorilla); thin supraorbital costae (Pongo) Neither Orbital shape Superiorly-inferiorly elongate/ovoid (Pongo) Pan/Gorilla Interorbital septum Relatively narrow in relation to biorbital breadth (Pongo) Pan/Gorilla Infraorbital foramina Positioned well medial to zygomatico-maxillary suture at orbit (Pongo) Pan/Gorilla Malar orientation Gradually posteriorly convex (Pan/Gorilla) Pongo Nasoalveolar clivus Strongly convex antero-posteriorly and highly prognathic (Pongo) Pan Subnasal topography Minimal offset from nasoalveolar clivus to nasal ﬂoor (Pongo) Pan/Gorilla Incisive canal Highly restricted (Pongo) Pan/Gorilla Midfacial proﬁle Continuously concave from glabella to nasospinale (Pongo) Pan Frontal sinus Absent (Pongo) Pan/Gorilla

several species of deinotheres, anthracotheres, rhinoceroses, and and East Asia, there was greater suprageneric taxonomic di- suids, whereas there are no ungulate species in common between versity among apes than recognized in most recent taxonomies. the South/Southeast Asian faunas and those from southern China (25, 26, 28–30). Although these faunal patterns do not bear di- Materials and Methods rectly upon the question of whether Lufengpithecus is a member A database was assembled of metric and nonmetric characters for extant of the Pongo clade, they do underscore that the fossil apes great apes of approximately the same stage of dental development as showing clear links to the Pongo clade occur in faunal contexts YV0999. The database included 10 specimens of Pan troglodytes troglodytes, – that are strikingly different from those at Yuanmou or Shihuiba. 9 specimens of Gorilla gorilla gorilla (both samples from the Hamman Todd collection at the Cleveland Museum of Natural History), and 11 specimens of The pattern of faunal differences between southern China Pongo pygmaeus pygmaeus (2 from the Hamman–Todd collection and 9 and South/Southeast Asia further suggests the possibility of dif- from the Zoologische Staatssammlung, München, Germany). ferent dispersal routes of apes into East Asia earlier in the Mio- Measurements were selected based on the preservation of YV0999. For cene: one route through the South Asian subcontinent and thence YV0999, unilateral measurements were taken on the right side or in the into Southeast Asia (members of the Pongo lineage) and a more midline. Some bilateral measurements were calculated by doubling the right- northern route between Europe and southern China through west side measurement. Raw measurements from the great ape crania and YV0999 central China before uplift of the northern Tibetan Plateau. were converted to Mossiman shape variables (38) to control for size differ- Various lines of evidence indicate that major uplift of the northern ences among the different taxa. This involves calculating the geometric regions of the plateau occurred substantially later than in the mean (GM) for each specimen and dividing the raw measurements by the geometric mean. Variables were ﬁrst log-transformed and the shape varia- south, which would have led to a more prolonged period of bles calculated as log(y) − log(GM). equable climatic conditions conducive to faunal dispersal through Eighteen measurements were used in both the cluster and discriminant central Asia, at least into the early late Miocene (31–35). analyses of the crania to explore overall resemblance in cranial shape irre- In light of these possibilities, comparisons between Lufengpi- spective of cladistic criteria (SI Text). Both were carried out using SYSTAT thecus and European Miocene apes, particularly Rudapithecus 10.0. The cluster analysis incorporated the Join function. The distance metric from eastern Europe, a possible member of the African ape/ in this procedure is Euclidean distance. A single bivariate analysis of orbital human clade (16, 17), and between their respective faunas, might shape and relative interorbital distance was also carried out (Fig. S2) because prove informative. They could help resolve the question of of the clear apomorphic condition of these features in extant Pongo. Rela- whether Lufengpithecus is a stem hominid or a member of the tive interorbital distance equals the minimum interorbital width divided by the maximum distance in the orbital plane from the midnasal suture to the African ape/human clade. Preliminary dental comparisons be- lateral margin of the zygomatico-frontal orbital pillar unilaterally. Orbital tween Lufengpithecus and Rudapithecus have revealed a number shape equals maximum orbital height divided by maximum orbital width. of similarities (36). For example, Lufengpithecus shares with Relative interorbital distance and orbital shape were both calculated using Rudapithecus, and with most other western European Miocene unscaled raw measurements. apes, very slender lower canines and a distinctive upper central incisor morphology with a relatively narrow crown and a prom- ACKNOWLEDGMENTS. We thank Dr. Richard Kraft, Director of the Zoologi- inent lingual pillar (1, 15, 17, 21, 36, 37). Although the phylo- sche Staatssammlung, München; Dr. Yohannes Haile-Selassie, Curator of ﬁ Physical Anthropology; and Lyman Jellema, collections manager at the genetic af nities of Lufengpithecus are not yet certain, its Cleveland Museum of Natural History for allowing us to examine specimens morphology demonstrates that during the late Miocene in South housed at their institutions. We also thank Liu Xu, Director, and Yang

Table 2. Faunal comparison between late Miocene hominoid sites in southern China (Yuanmou, Shihuiba), South Asia (Siwaliks), and Southeast Asia (Khorat, Irrawaddy Formation) Yuanmou Shihuiba Siwaliks Khorat Irrawaddy Formation

Ursidae Present Present Absent Absent Absent Deinotheriidae Absent Absent Present Present Absent Tapiridae Present Present Absent Absent Absent Suidae Present Present Same species Same species Same species Anthracotheriidae Absent Absent Present Present Present Tragulidae Present Present Abundant, diverse ? Present Girafﬁdae Absent Absent Present Present Present Bovidae Absent or rare Low diversity Abundant, diverse Abundant Diverse Cervidae Abundant, diverse Abundant, diverse Absent Absent Absent

Data are from Refs. 25, 26, 28–30.

6884 | www.pnas.org/cgi/doi/10.1073/pnas.1201330109 Kelley and Gao Downloaded by guest on September 28, 2021 Decong, former Director, of the Yunnan Institute of Cultural Relics and Ar- the invitation to study YV0999. We thank Dr. Gary Schwartz and Dr. Steve chaeology for ﬁnancial and logistical support. J.K. thanks Liu Wu of the Ward for discussions. J.K. was supported by the College of Dentistry, Univer- Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, for sity of Illinois at Chicago.

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