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A Unique Middle Miocene European Hominoid and the Origins of the Great Ape and Human Clade

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A unique Middle Miocene European hominoid and the origins of the great ape and human clade Salvador Moya` -Sola` a,1, David M. Albab,c, Sergio Alme´ cijac, Isaac Casanovas-Vilarc, Meike Ko¨ hlera, Soledad De Esteban-Trivignoc, Josep M. Roblesc,d, Jordi Galindoc, and Josep Fortunyc aInstitucio´Catalana de Recerca i Estudis Avanc¸ats at Institut Catala`de Paleontologia (ICP) and Unitat d’Antropologia Biolo`gica (Dipartimento de Biologia Animal, Biologia Vegetal, i Ecologia), Universitat Auto`noma de Barcelona, Edifici ICP, Campus de Bellaterra s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain; bDipartimento di Scienze della Terra, Universita`degli Studi di Firenze, Via G. La Pira 4, 50121 Florence, Italy; cInstitut Catala`de Paleontologia, Universitat Auto`noma de Barcelona, Edifici ICP, Campus de Bellaterra s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain; and dFOSSILIA Serveis Paleontolo`gics i Geolo`gics, S.L. c/ Jaume I nu´m 87, 1er 5a, 08470 Sant Celoni, Barcelona, Spain Edited by David Pilbeam, Harvard University, Cambridge, MA, and approved March 4, 2009 (received for review November 20, 2008) The great ape and human clade (Primates: Hominidae) currently sediments by the diggers and bulldozers. After 6 years of includes orangutans, gorillas, chimpanzees, bonobos, and humans. fieldwork, 150 fossiliferous localities have been sampled from the When, where, and from which taxon hominids evolved are among 300-m-thick local stratigraphic series of ACM, which spans an the most exciting questions yet to be resolved. Within the Afro- interval of 1 million years (Ϸ12.5–11.3 Ma, Late Aragonian, pithecidae, the Kenyapithecinae (Kenyapithecini ؉ Equatorini) Middle Miocene). To date, 38,000 macrovertebrate remains and have been proposed as the sister taxon of hominids, but thus far thousands of small mammal teeth have been recovered from the the fragmentary and scarce Middle Miocene fossil record has above mentioned localities, some of which have yielded primate hampered testing this hypothesis. Here we describe a male partial remains (3–5). These localities can be accurately dated because face with mandible of a previously undescribed fossil hominid, of detailed litho-, bio-, and magnetostratigraphic control (4). An Anoiapithecus brevirostris gen. et sp. nov., from the Middle Mio- age close to 11.9 Ma can be estimated for ACM/C3-Aj, from cene (11.9 Ma) of Spain, which enables testing this hypothesis. which IPS43000 was excavated. Morphological and geometric morphometrics analyses of this ma- terial show a unique facial pattern for hominoids. This taxon Description. The face of IPS43000 (Fig. 1) lacks the nasals and the ANTHROPOLOGY combines autapomorphic features—such as a strongly reduced right maxilla, some parts of the orbits, and parts of both facial prognathism—with kenyapithecine (more specifically, keny- zygomatics. The palate is nearly complete, lacking only the left apithecin) and hominid synapomorphies. This combination sup- C1 and M3, as well as the incisors; part of the frontal also is ports a sister-group relationship between kenyapithecins (Gripho- preserved. The mandible preserves the symphysis and a large pithecus ؉ Kenyapithecus) and hominids. The presence of both portion of the 2 corpora, but lacks the 2 rami; the left I1 and groups in Eurasia during the Middle Miocene and the retention in C1-M2 series and the right C1-M1 series are preserved. Complete kenyapithecins of a primitive hominoid postcranial body plan eruption of the M3 indicates that IPS43000 belongs to an adult support a Eurasian origin of the Hominidae. Alternatively, the two individual, because the slight displacement of this tooth from the extant hominid clades (Homininae and Ponginae) might have alveolar plane merely results from bone distortion at the level of independently evolved in Africa and Eurasia from an ancestral, M2-M3. Middle Miocene stock, so that the supposed crown-hominid syna- pomorphies might be homoplastic. Systematic Paleontology. Systematic paleontology is as follows: Order Primates Linnaeus, 1758; suborder Anthropoidea Mivart, ͉ ͉ ͉ ͉ Anoiapithecus gen. nov. evolution Hominidae Hominoidea 1864; infraorder Catarrhini Geoffroy, 1812; superfamily Homi- Paleoprimatology noidea Gray, 1825; family Hominidae Gray, 1825; subfamily incer- tae sedis; tribe Dryopithecini Gregory and Hellman, 1939; Anoia- here is a general consensus on the relevance of Middle pithecus gen. nov. type species A. brevirostris gen. et sp. nov. TMiocene hominoids for understanding hominid origins (1, Etymology is from Anoia (the region where the site is situated) and 2). However, the question of the initial great-ape/human radi- the Greek pithekos (ape). Generic diagnosis is as for the type ation still remains elusive. In this paper we describe a previously species, A. brevirostris gen. et sp. nov. Holotype is IPS43000, a partial underscribed Middle Miocene thick-enameled hominid [see face with mandible of an adult male individual, housed at the supporting information (SI) Text and Table S1, regarding the Institut Catala`de Paleontologia (Fig. 1; see Table 1 for dental systematic framework used in this paper], which displays a measurements). Type locality is ACM/C3-Aj (Abocador de Can unique and unusual combination of facial characteristics with Mata, Cell 3, locality Aj), in the municipal term of Els Hostalets de significant phylogenetic implications. Anoiapithecus brevirostris Pierola (Catalonia, Spain). Age is subchron C5r.3r (Middle Mio- gen. et sp. nov. shows the basic great-ape synapomorphies and cene, Ϸ11.9 Ma), on the basis of the local ACM magnetostrati- some generalized afropithecid and several kenyapithecine- graphic series (4), corresponding to the local biozone Megacricet- derived features, coupled with a striking reduction of the face. odon ibericus ϩ Democricetodon larteti (MN 7 Mammal Neogene This combination is unknown from any fossil or extant great ape, biozone), on the basis of biostratigraphic data (3, 4). Etymology is which has important implications for reconstructing the initial from the Latin brevis (short) and rostrum (snout). evolutionary history of the great ape and human clade. Stratigraphic Setting. The description of this taxon is based on a Author contributions: S.M.-S. designed research; S.M.-S., D.M.A., and M.K. performed hominoid partial face with mandible (IPS43000) discovered at research; J.F. contributed new reagents/analytic tools; D.M.A., S.A., I.C.-V., S.D.E.-T., J.M.R., locality Abocador de Can Mata (ACM)/C3-Aj, in the area of Els J.G., and J.F. analyzed data; and S.M.-S., D.M.A., and M.K. wrote the paper. Hostalets de Pierola (Valle`s-Penede`s Basin, Catalonia, Spain). Conflict of interest: The authors declare no conflict of interest. This region is characterized by thick Middle to Late Miocene This article is a PNAS Direct Submission. stratigraphic sequences. The construction of a rubbish dump 1To whom correspondence should be addressed. E-mail: [email protected]. (ACM) near the country house of Can Mata (Fig. S1) prompted This article contains supporting information online at www.pnas.org/cgi/content/full/ a paleontological intervention to control the removal of Miocene 0811730106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811730106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 26, 2021 AB CD E F G Fig. 1. Cranium and mandible of Anoiapithecus brevirostris (IPS43000, holotype). (A) Right lateral view. (B) Frontal view. (C) Left lateral view. (D) Superior view. (E) Palatal view. (F) Occlusal view of the mandible. (G) CT scan of the right M2, showing enamel thickness. All photographs were taken with the tooth row oriented horizontally. For safety reasons, the cranial reconstruction (A–D) is based on casts of the original specimens. Specific Diagnosis. The face is characterized by reduced nasal and the posterior part of the C1 (with the alveolar plane horizontal). alveolar prognathism with a very short premaxilla. The anterior Nasal aperture edges are vertical. The zygomatic root is mod- border of the orbit is situated over the P3–P4 limit, the glabella erately high and situated over the M1. The anterior surface of the is over the P4, and the anteriormost nasomaxillary contact is over zygomatic root is downwardly inclined. The frontal sinus is well developed, filling the glabellar area and part of the frontal squama. The maxillary sinus is reduced, situated well above the Table 1. Dental measurements (in millimeters) of Anoiapithecus roots of the molars, occupying a small area below the medial side brevirostris gen. et sp. nov. from ACM/C3-Aj of the orbit. The zygomatic root is not pneumatized. Coalescent Upper teeth Lower teeth temporal lines indicate the presence of a sagittal crest. Thin superciliary arches are evident. A large and open incisive MD BL MD BL foramen, with the posterior border located at the level of the P3, is shown. The palate is short, wide, and deep. The pyriform L I1 — — 4.8 6.7 aperture is wide, widest close to the base. Dentition is charac- R C1 14.2 9.6 12.9 8.5 ϭ L C1 — — 13.2 9.2 terized by thick enamel (relative enamel thickness, RET 20) R P3 — — 12.7 7.3 with low dentine penetrance. Low crowns show globulous cusps, L P3 7.0 11.7 12.3 7.6 blunt crests, and restricted basins with nonperipheralized cusps; R P4 — — 7.6 8.8 there are remnants of cingula in lower teeth. Canines and P3 are L P4 7.2 10.4 7.8 8.6 low-crowned whereas upper canines are relatively small and very R M1 9.4 11.2 9.1 8.9 compressed. A robust mandible shows highly divergent rami and L M1 9.4 11.4 9.5 9.1 reduced mandibular length; strong and long inferior torus and R M2 11.3 11.8 — — weak superior torus that forms a simian shelf. L M2 10.7 12.1 11.5 10.0 R M3 10.2 10.4 — — Differential Diagnosis.
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  • Simian Malaria in the Brazilian Atlantic Forest: First Description of Natural Infection of Capuchin Monkeys (Cebinae Subfamily) by Plasmodium Simium

    Simian Malaria in the Brazilian Atlantic Forest: First Description of Natural Infection of Capuchin Monkeys (Cebinae Subfamily) by Plasmodium Simium

    de Alvarenga et al. Malaria Journal (2015) 14:81 DOI 10.1186/s12936-015-0606-6 RESEARCH Open Access Simian malaria in the Brazilian Atlantic forest: first description of natural infection of capuchin monkeys (Cebinae subfamily) by Plasmodium simium Denise Anete Madureira de Alvarenga1, Anielle de Pina-Costa2,3, Taís Nóbrega de Sousa1, Alcides Pissinatti4,5, Mariano G Zalis6, Martha C Suaréz-Mutis7, Ricardo Lourenço-de-Oliveira8, Patrícia Brasil2, Cláudio Tadeu Daniel-Ribeiro3,9 and Cristiana Ferreira Alves de Brito1* Abstract Background: In Brazil, two species of Plasmodium have been described infecting non-human primates, Plasmodium brasilianum and Plasmodium simium. These species are morphologically, genetically and immunologically indistinguishable from the human Plasmodium malariae and Plasmodium vivax parasites, respectively. Plasmodium simium has been observed naturally infecting monkeys of the genera Alouatta and Brachyteles in a restricted area of the Atlantic Forest in the south and southeast regions of Brazil. However, its reported geographical distribution and the diversity of its vertebrate hosts may be underestimated, since available data were largely based on analyses by microscopic examination of peripheral blood, a method with limited sensitivity, considering the potential sub-patent feature of these infections. The present study describes, for the first time, the natural infection of P. simium in capuchin monkeys from the Brazilian Atlantic Forest. Methods: Blood samples from 30 non-human primates belonging to nine species kept in the Primate Centre of Rio de Janeiro were collected. Fragments of spleen and liver from one dead monkey found in the neighborhoods of the Primate Centre were also analysed. Molecular diagnosis was performed by nested PCR (18SSU rRNA) and the amplified fragment was sequenced.