First North American fossil monkey and early Miocene tropical biotic interchange

Abstract

New World monkeys (platyrrhines) are a diverse part of modern tropical ecosystems in North and South America, yet their early evolutionary history in the tropics is largely unknown. Molecular divergence estimates suggest that primates arrived in tropical Central America, the southern-most extent of the North American landmass, with several dispersals from South America starting with the emergence of the Isthmus of Panama 3–4 million years ago (Ma)1. The complete absence of primate fossils from Central America has, however, limited our understanding of their history in the New World. Here we present the first description of a fossil monkey recovered from the North American landmass, the oldest known crown platyrrhine, from a precisely dated 20.9-Ma layer in the Las Cascadas Formation in the Panama Canal Basin, Panama. This discovery suggests that family-level diversification of extant New World monkeys occurred in the tropics, with new divergence estimates for Cebidae between 22 and 25 Ma, and provides the oldest fossil evidence for mammalian interchange between South and North America. The timing is consistent with recent tectonic reconstructions2,3 of a relatively narrow Central American Seaway in the early Miocene epoch, coincident with over-water dispersals inferred for many other groups of animals and plants4. Discovery of an early Miocene primate in Panama provides evidence for a circum-Caribbean tropical distribution of New World monkeys by this time, with ocean barriers not wholly restricting their northward movements, requiring a complex set of ecological factors to explain their absence in well-sampled similarly aged localities at higher latitudes of North America.

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Figure 1: Stratigraphy of the primate-bearing locality (YPA-024) in central Panama.
Figure 2: Comparison of Panamacebus with middle Miocene cebid Neosaimiri fieldsi from La Venta, Colombia.
Figure 3: Results from phylogenetic analyses showing Panamacebus within crown Platyrrhini.
Figure 4: Palaeogeographic reconstruction showing hypothetical dispersal route of Panamacebus across the CAS in the early Miocene.

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Acknowledgements

We thank M. Silcox, D. Boyer, G. Gunnell, S. Chester, P. Morse, E. Sargis, D. Steadman, E. Kowalski, Z. Randall, A. Rosenberger, J. Krigbaum and D. Daegling for advice and discussion, R. Kay and L. Marivaux for reviews that significantly improved the quality of the manuscript, D. Byerley and G. Maccracken for finding primate fossils in Panama, M. Droulliard for assistance with geochronology laboratory and fieldwork, R. Kay, P. Holroyd and D. Reed for access to comparative specimens, J. Bourque for fossil preparation, D. Byerley for artwork associated with Fig. 3, D. Boyer for facilitating access to the Duke University SMIF microCT facility, and D. Boyer, G. Yapuncich and J. Thostenson for help acquiring and processing microCT scan data (funded in part by National Science Foundation (NSF) BCS 1304045 to D. Boyer and E. St Clair, and BCS 0851272 to R. Kay). We thank O. Moskalenko, M. Gitzendanner and D. Reed for assistance with the high-performance computing resources at the University of Florida. We thank the Autoridad del Canal de Panama (ACP) and the Ministerio de Comercio e Industria (MICI) for logistical support and access to the Panama Canal Zone. Part of this manuscript was written when J.I.B. was supported as an Edward P. Bass Distinguished Visiting Environmental Scholar in the Yale Institute for Biospheric Studies (YIBS). The NSF (PIRE project 0966884), Smithsonian Tropical Research Institute Paleobiology Fund, and the Florida Museum of Natural History funded this research. This is University of Florida Contribution to Paleobiology 782.

Author information

Affiliations

Authors

Contributions

J.I.B., A.R.W., E.D.W. and G.S.M. contributed to project planning. J.I.B., A.R.W. and A.R.H. contributed to systematic palaeontology and microCT scans. D.A.F. and A.F.R. contributed to radioisotopic analyses and stratigraphy. B.J.M., A.F.R., G.S.M., A.R.W. and J.I.B. contributed to biochronological analysis. E.D.W., J.I.B. and A.R.W. contributed to phylogenetic analyses. E.D.W. performed divergence dating analyses. C.M. and C.A.J. contributed to palaeogeographic analysis. N.A.J., J.I.B. and C.A.J. contributed to the pollen summary. A.R.W., A.F.R., J.I.B., G.S.M., E.D.W. and D.S.J. contributed to fieldwork. J.I.B., B.J.M., G.S.M., C.A.J. and D.S.J. contributed to financial support. All authors contributed to manuscript and figure preparation.

Corresponding author

Correspondence to Jonathan I. Bloch.

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The authors declare no competing financial interests.

Additional information

The LSIDs for Panamacebus (genus), urn:lsid:zoobank.org:act:C33F8967-EE79-47B8-8A98-2C6D2C7557CA, and for Panamacebus transitus (species), urn:lsid:zoobank.org:act:3E01F3F2-B1F8-433E-B110-9AD5AAF3DB99, have been deposited in ZooBank.

Extended data figures and tables

Extended Data Figure 1 Map of the southern part of Panama Canal (Gaillard Cut).

Black circles mark the position of the Lirio Norte Local Fauna locality (YPA024) and other specific terrestrial vertebrate collecting sites (Centenario Fauna) in the area (modified from ref. 10).

Extended Data Figure 2 Photograph of the northern wall (south-facing) in the Lirio Norte Local Fauna locality (YPA024).

Dated rock sample MD11 was collected from an ash layer that forms the upper-most part of a several-metre thick, welded andesitic tuff. The tuff is exposed within the conformable section of the Las Cascadas Formation approximately 0.25 m below, and in close proximity to, the mammal fossil-bearing unit that includes the Panamacebus fossils.

Extended Data Figure 3 Generic-level biostratigraphy of selected taxa from the early Miocene (~21 Ma) Las Cascadas Formation, Panama.

Individual biochronologies were interpreted from temporal ranges known from higher-latitudes. The calibration of the NALMA boundaries is as described previously13,14.

Extended Data Figure 4 Detailed upper molar comparisons of Panamacebus to Neosaimiri.

ad, Left to right, occlusal, distal, lingual, mesial and buccal views of the left M1 (UF 280128: http://dx.doi.org/10.17602/M2/M8531) (a) and the left M2 (UF 281001: http://dx.doi.org/10.17602/M2/M8550) (d) of P. transitus compared with M1 and M2 of N. fieldsi (b, c, eg): right M1 (IGM-KU 89008: http://dx.doi.org/10.17602/M2/M8541) (b), right M1 (IGM 89019: http://dx.doi.org/10.17602/M2/M8544) (c), right M2 (IGM-KU 89018: http://dx.doi.org/10.17602/M2/M8543) (e), right M2 (IGM-KU 89104: http://dx.doi.org/10.17602/M2/M8548) (f), and right M2 (IGM-KU 89011: http://dx.doi.org/10.17602/M2/M8542) (g). Images were generated from microCT scan data (see Methods and links associated with specimen numbers). Right-sided teeth were flipped to facilitate comparison with left-sided teeth. Scale bar, 1 mm.

Extended Data Figure 5 Detailed upper molar comparisons of Panamacebus to Neosaimiri and Cebus.

ag, Left to right, occlusal, distal, lingual, mesial and buccal views of the left M1 (UF 280128: http://dx.doi.org/10.17602/M2/M8531) (a) and the left M2 (UF 281001: http://dx.doi.org/10.17602/M2/M8550) (c) of P. transitus compared with M1 and M2 of N. fieldsi (b, d): right M1 (IGM 89019: http://dx.doi.org/10.17602/M2/M8544) (b), and right M2 (IGM-KU 89104: http://dx.doi.org/10.17602/M2/M8548) (d); and the left M1 and M2 of Cebus capucinus (USNM 291128; http://dx.doi.org/10.17602/M2/M8627) in occlusal (e), lingual (f) and buccal views (g). Images were generated from microCT scan data (see Methods and links associated with specimen numbers). Right-sided teeth were flipped to facilitate comparison with left-sided teeth. Scale bar, 1 mm.

Extended Data Figure 6 Detailed comparisons of Panamacebus lower teeth to those of Neosaimiri and Stirtonia.

ak, Left to right, occlusal, distal, lingual, mesial and buccal views of the partial left I1 (UF 280130: http://dx.doi.org/10.17602/M2/M8400) (a), right I2 (UF 267048, mirrored: http://dx.doi.org/10.17602/M2/M8395) (d), left P2 (UF 280127: http://dx.doi.org/10.17602/M2/M8397) (g), left P4 (UF 280129: http://dx.doi.org/10.17602/M2/M8399) (i) and right C1 (UF 280131, mirrored: http://dx.doi.org/10.17602/M2/M8401) (k) of P. transitus compared with the right I1 (IGM-KU 89086: http://dx.doi.org/10.17602/M2/M8546) (b), right I2 (IGM-KU 89092: http://dx.doi.org/10.17602/M2/M8547) (e), left I2 (UCMP 39205: http://dx.doi.org/10.17602/M2/M1880) (f), right P2 (IGM-KU 90016: http://dx.doi.org/10.17602/M2/M8549) (h) and right C1 (IGM-KU 89021: http://dx.doi.org/10.17602/M2/M8432) (j) of N. fieldsi and the right I2 (UCMP 38989: http://dx.doi.org/10.17602/M2/M1799) of Stirtonia tatacoensis (c). Images were generated from microCT scan data (see Methods and links associated with specimen numbers). Right-sided teeth were flipped to facilitate comparison with left-sided teeth. Scale bar, 5 mm.

Extended Data Figure 7 Detailed comparisons of Panamacebus lower teeth to those of Cebus.

ai, Occlusal (a), lingual (c) and buccal (e) views of P. transitus partial left I1 (UF 280130: http://dx.doi.org/10.17602/M2/M8400), right I2 (UF 267048, mirrored: http://dx.doi.org/10.17602/M2/M8395), right C1 (UF 280131, mirrored: http://dx.doi.org/10.17602/M2/M8401), left P2 (UF 280127: http://dx.doi.org/10.17602/M2/M8397) and left P4 (UF 280129: http://dx.doi.org/10.17602/M2/M8399); occlusal (b), lingual (d) and buccal (f) views of C. capucinus right P2–P4 (USNM 291128: http://dx.doi.org/10.17602/M2/M8629); and occlusal (g), lingual (h) and buccal (i) views of C. capucinus left dentary with I1–M3 (USNM 291236: http://dx.doi.org/10.17602/M2/M8622). Right-sided teeth were mirrored to facilitate comparison with left-sided teeth. Images were generated from microCT scan data (see Methods). Scale bars, 5 mm.

Extended Data Figure 8 Detailed palaeogeographic reconstruction of the Panama Canal Basin region during the late Oligocene–early Miocene, showing the location of key geological formations, faults and tectonic blocks.

Sedimentary environments were extrapolated from published stratigraphic sections that were placed over the palinspastic reconstruction in the following locations: (1) Pacific sections that include conglomerate and sandy strata; (2) upper Magdalena Basin; (3) Amaga Formation coal-bearing and sandy-conglomeratic; (4) Choco; (5) easternmost Panama; 96) western Panama; (7) Panama; (8) Canal basin; (9) northwestern Colombia; (10) Sierra Nevada Santa Marta, unnamed sandy and conglomeratic strata; (11) Guajira Peninsula; (12) Falcon; (13) Falcon/Lara; (14) middle Magdalena Basin; (15) Floresta Massif; (16) axial Cordillera Oriental; (17) foothills; (18) southern middle Magdalena Basin. See Supplementary Methods for references and detailed discussion.

Extended Data Figure 9 Maximum clade credibility tree summarizing the concatenated trees from the divergence dating analysis using the birth–death model showing the Platyrrhini.

Ninety-five per cent highest posterior density intervals are shown on key nodes and the corresponding branches are labelled with posterior probability values. For clarity, only the Platyrrhini are shown here.

Extended Data Figure 10 Maximum clade credibility tree summarizing the concatenated trees from divergence dating the analysis using the Yule model showing the Platyrrhini.

Ninety-five per cent highest posterior density intervals are shown on key nodes and the corresponding branches are labelled with posterior probability values. For clarity, only the Platyrrhini are shown here.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-10 comprising: an illustration of cusp and crest nomenclature (Figure 1), images from micro CT scans of upper and lower dentitions of Cebupithecia and Stirtonia from the middle Miocene of Colombia (Figures 2-3) and phylogenetic trees resulting from maximum parsimony analyses of Panamacebus (Figures 4-10). (PDF 1652 kb)

Supplementary Methods and Results

This file contains detailed Methods and additional morphological comparisons of Panamacebus to other primates and detailed Methods and Results of stratigraphic, geochronological, phylogenetic, and divergence analyses, and paleobotanical reconstructions. (PDF 1005 kb)

Supplementary Tables

This zipped file contains Supplementary Tables 1-7 comprising: (1) U-Pb ages from individual magmatic zircons used to estimate the absolute date of the fossiliferous horizon where the Panamacebus fossils were discovered; (2) List of the prior node calibrations used for the divergence dating analysis in BEAST; (3) Pollen locality and richness data used in the paleobotanical reconstruction; (4) Scan settings for the micro CT scans presented in this paper; (5) Table of summary statistics from the divergence dating analyses in BEAST; (6) Mammalian faunal list from the Lirio Norte L. F. (YPA024), Las Cascadas Formation, Panama; (7) Biogeographic affinities and richness of Oligocene to middle Miocene pollen-bearing formations in Florida, Puerto Rico, southern Mexico, Costa Rica, and Panama. (ZIP 285 kb)

Supplementary Data

This zipped file contains Supplementary Data 1-4 comprising: (1) The morphological character-taxon matrix (in Nexus format) used in the parsimony analysis containing the new taxon, Panamacebus, and lists of ordered characters and weighted characters; (2) The molecular constraint tree used in the second phylogenetic analysis, presented in Nexus format; (3) The reduced sequence alignment used in the divergence dating analysis, presented in Phylip format;(4) List of all taxa included in each clade calibrated with a prior in the divergence dating analysis. (ZIP 1923 kb)

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Bloch, J., Woodruff, E., Wood, A. et al. First North American fossil monkey and early Miocene tropical biotic interchange. Nature 533, 243–246 (2016). https://doi.org/10.1038/nature17415

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