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First North American Fossil Monkey and Early Miocene Tropical Biotic Interchange Jonathan I

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First North American Fossil Monkey and Early Miocene Tropical Biotic Interchange Jonathan I LETTER doi:10.1038/nature17415 First North American fossil monkey and early Miocene tropical biotic interchange Jonathan I. Bloch1, Emily D. Woodruff1,2, Aaron R. Wood1,3, Aldo F. Rincon1,4, Arianna R. Harrington1,2,5, Gary S. Morgan6, David A. Foster4, Camilo Montes7, Carlos A. Jaramillo8, Nathan A. Jud1, Douglas S. Jones1 & Bruce J. MacFadden1 New World monkeys (platyrrhines) are a diverse part of modern Primates Linnaeus, 1758 tropical ecosystems in North and South America, yet their early Anthropoidea Mivart, 1864 evolutionary history in the tropics is largely unknown. Molecular Platyrrhini Geoffroy, 1812 divergence estimates suggest that primates arrived in tropical Cebidae Bonaparte, 1831 Central America, the southern-most extent of the North American Panamacebus transitus gen. et sp. nov. landmass, with several dispersals from South America starting with the emergence of the Isthmus of Panama 3–4 million years Etymology. Generic name combines ‘Panama’ with ‘Cebus’, root taxon ago (Ma)1. The complete absence of primate fossils from Central for Cebidae. Specific name ‘transit’ (Latin, crossing) refers to its implied America has, however, limited our understanding of their history early Miocene dispersal between South and North America. in the New World. Here we present the first description of a fossil Holotype. UF 280128, left upper first molar (M1; Fig. 2a, b). monkey recovered from the North American landmass, the oldest Referred material. Left upper second molar (M2; UF 281001; Fig. 2a, b), known crown platyrrhine, from a precisely dated 20.9-Ma layer in partial left lower first incisor (I1; UF 280130), right lower second the Las Cascadas Formation in the Panama Canal Basin, Panama. incisor (I2; UF 267048), right lower canine (C1; UF 280131), possibly This discovery suggests that family-level diversification of extant associated left lower second (P2; UF 280127) and fourth (P4; UF New World monkeys occurred in the tropics, with new divergence 280129) premolars (Fig. 2e–g). estimates for Cebidae between 22 and 25 Ma, and provides the Locality. Lirio Norte (site key YPA-024 in the Florida Museum of oldest fossil evidence for mammalian interchange between South Natural History Vertebrate Paleontology Collection), Panama Canal and North America. The timing is consistent with recent tectonic area, Panama, Central America (Extended Data Fig. 1). reconstructions2,3 of a relatively narrow Central American Seaway Age and horizon. Primate fossils were collected from a single horizon in the early Miocene epoch, coincident with over-water dispersals of sub-aerially exposed ash fall deposits in the upper part of the Las inferred for many other groups of animals and plants4. Discovery Cascadas Formation (Fig. 1a). Magmatic zircons from a non-subaerially of an early Miocene primate in Panama provides evidence for a exposed andesitic tuff, ~ 0.25 m below the primate-bearing horizon circum-Caribbean tropical distribution of New World monkeys by (Extended Data Fig. 2), yield an age of 20.93 ±​ 0.17 Ma (2σ) (Fig. 1b and this time, with ocean barriers not wholly restricting their northward Supplementary Table 1), interpreted to be the eruption age of the tuff and movements, requiring a complex set of ecological factors to explain a close approximation of the absolute age of the primate-bearing horizon. their absence in well-sampled similarly aged localities at higher The mammalian assemblage (Supplementary Table 6) recovered from latitudes of North America. this horizon is consistent with what is known from the late Arikareean The Miocene epoch (23.8–5.3 Ma) is marked by substantial climatic Ar4 faunal zone (22.8–19.05 Ma; refs 10, 13) North American Land and ecological changes that had profound effects on terrestrial mam- Mammal Age (NALMA) at higher latitudes13,14 (Extended Data Fig. 3). mal communities in the New World tropics5. Fossils from the tropical See also Supplementary Information (results section). lowlands of Central America are rare owing to a lack of relevant rock Diagnosis. Medium-sized cebid platyrrhine (~ 2.7 kg) that differs exposures; however, an important exception can be found in Panama from all other cebines in having lower incisors (I1, I2) that are higher where, since 2009, expansion of the Panama Canal has exposed fossil- crowned with an incomplete lingual cingulum, and a first upper bearing rocks of early Miocene age. The lower Miocene Las Cascadas molar (M1) that is considerably larger than the second upper molar Formation (Fig. 1) represents the oldest fossiliferous continental (M2). Further differs from most cebines: (except Aotus) in having 3 sequence exposed along the Panama Canal area and includes a diverse an I1 cross-sectional area only somewhat smaller than that of I2; 6–9 fossil mammal assemblage that, while compositionally different (except Cebus) in having somewhat inflated lower premolars (P2, P4), 10 from that of the younger overlying Centenario Fauna , similarly has and a P4 talonid and trigonid of similar length; and (except Saimiri almost entirely North American affinities despite its proximity to South and Neosaimiri) in having M1,2 with a short and strong anterior America, consistent with a peninsular connection to North America10,11. cingulum. Further differs: from Cebus and Acrecebus in having M1,2 Palaeontological fieldwork in 2012–2013 resulted in the discovery of with a mesiobuccally oriented prehypocrista, lacking a metaconule, a seven isolated fossil primate teeth that shed new light on the early postprotocrista that is continuous with a hypometacrista that reaches evolution of crown New World monkeys in the tropics and pro- to the base of the metacone, a sharp and distinct hypometacrista, vide insight into the timing and dynamics of the earliest stages of the and lack of lingual inflation of the protocone; from Cebus in having Great American Biotic Interchange (GABI) between North and South a P4 with a smaller hypoconid; and from Saimiri in lacking a America12. pericone on M1,2. Differs from all callitrichines in having a discrete 1Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800, USA. 2Department of Biology, University of Florida, Gainesville, Florida 32611-7800, USA. 3Department of Geological and Atmospheric Sciences, Iowa State University, Ames, Iowa 50011-1027, USA. 4Department of Geological Sciences, University of Florida, Gainesville, Florida 32611-7800, USA. 5Department of Evolutionary Anthropology, Duke University, Durham, North Carolina 27708-9976, USA. 6New Mexico Museum of Natural History and Science, Albuquerque, New Mexico 87104, USA. 7Geociencias, Universidad de los Andes, Calle 1A # 18A-10, Edificio IP, Bogotá DC 111711, Colombia. 8Smithsonian Tropical Research Institute, Box 0843-03092, Balboa, Ancon, Republic of Panama. 00 MONTH 2016 | VOL 000 | NATURE | 1 © 2016 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER a ab cd 15 Fm. Pedro Miguel Ma Epoch Biochronol. 16 . He2 Cucaracha Formation eh Centenario Fauna (~19 Ma) He1 18 Hemingf e 19.29 ± 0.4 Ma (a) Culebra 20 Formation Miocen Ar4 10 * f i 22 * 20.93 ± 0.17 Ma n Lirio Norte local fauna 24 Ar3 Arikareean 26 e Ar2 25.37 ± 0.13 Ma (b) Las Cascadas Formatio Oligocen 28 g j Ar1 o 5 Fm. Bas 30 Obisp b 25 Mean = * 20.93 ± 0.17 Ma . 24 MSWD = 0.85, probability = 0.73 23 22 U age (Ma) 21 238 / 20 Figure 2 | Comparison of Panamacebus with middle Miocene cebid Pb 206 19 Neosaimiri fieldsi from La Venta, Colombia. a, b, Occlusal (a) and 1 18 0 lingual (b) views of P. transitus left M (UF 280128: http://dx.doi. org/10.17602/M2/M8531) and M2 (UF 281001: http://dx.doi.org/10.17602/ 1 Purple–grey mudstones Ash falls and lapilli tuffs Fossil M2/M8550). c, d, Occlusal (c) and lingual (d) views of N. fieldsi right M Agglomerates Grey and black mudstones vertebrates (IGM-KU 89008, mirrored: http://dx.doi.org/10.17602/M2/M8541) and Conglomerates Sandstones M2 (IGM-KU 89018, mirrored: http://dx.doi.org/10.17602/M2/M8543). Figure 1 | Stratigraphy of the primate-bearing locality (YPA-024) in e–g, Occlusal (e), lingual (f) and buccal (g) views of P. transitus partial central Panama. a, Measured stratigraphic section (in metres) in the left I1 (UF 280130: http://dx.doi.org/10.17602/M2/M8400), right I2 (UF Las Cascadas Formation showing the positions of the dated rock sample 267048, mirrored: http://dx.doi.org/10.17602/M2/M8395), right C1 (UF (asterisk) and of the Panamacebus fossils as a silhouette of a monkey (right), 280131, mirrored: http://dx.doi.org/10.17602/M2/M8401), left P2 (UF correlated to a schematic stratigraphic position of the Lirio Norte Local 280127: http://dx.doi.org/10.17602/M2/M8397) and left P4 (UF 280129: Fauna and the Centenario Fauna with previously published radiometric http://dx.doi.org/10.17602/M2/M8399). h–j, Occlusal (h), lingual (i) and dates (a, ref. 3; b, ref. 28) indicated (centre), and North American land buccal (j) views of N. fieldsi left dentary with I2–M2 (UCMP 39205: http:// mammal faunal zonation (left). Biochronol., Biochronology; Fm., dx.doi.org/10.17602/M2/M1879, http://dx.doi.org/10.17602/M2/M1880). formation; Hemingf., Hemingfordian North American Land Mammal Age; Images generated from microCT scan data (see Methods and links MSWD, mean square of weighted deviates. b, Results from U–Pb isotopic associated with specimen numbers). Scale bars: 1 mm (a–d); 5 mm (e–j). analyses plotted as a weighted mean of the 206Pb/238U ages from 37 zircons (see Methods and Supplementary Information). for their arrival into South America19. Results from phylogenetic analyses of new morphological data coded into a previously published 1,2 1 1,20 entoconid on P4, and M with a large hypocone and lacking a matrix vary with the use of different molecular constraints , but buccal cingulum; from callitrichines (but also Aotus) in having an both support Panamacebus within crown Platyrrhini, specifically M2 with a buccally expanded paracone; and from callitrichines within Cebidae (Fig.
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