First North American fossil monkey and early Miocene tropical biotic interchange (original) (raw)

References

  1. Kay, R. F. Biogeography in deep time—what do phylogenetics, geology, and paleoclimate tell us about early platyrrhine evolution? Mol. Phylogenet. Evol. 82, 358–374 (2015)
    Article Google Scholar
  2. Farris, D. W. et al. Fracturing of the Panamanian Isthmus during initial collision with South America. Geology 39, 1007–1010 (2011)
    Article ADS CAS Google Scholar
  3. Montes, C. et al. Evidence for middle Eocene and younger land emergence in central Panama: implications for Isthmus closure. Geol. Soc. Am. Bull. 124, 780–799 (2012)
    Article ADS CAS Google Scholar
  4. Bacon, C. D. et al. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc. Natl Acad. Sci. USA 112, 6110–6115 (2015)
    Article ADS CAS Google Scholar
  5. MacFadden, B. J. Extinct mammalian biodiversity of the ancient New World tropics. Trends Ecol. Evol. 21, 157–165 (2006)
    Article Google Scholar
  6. Rincon, A. F., Bloch, J. I., Suarez, C., MacFadden, B. J. & Jaramillo, C. A. New floridatragulines (Mammalia, Camelidae) from the early Miocene Las Cascadas Formation, Panama. J. Vertebr. Paleontol. 32, 456–475 (2012)
    Article Google Scholar
  7. Rincon, A. F., Bloch, J. I., Macfadden, B. J. & Jaramillo, C. A. First Central American record of Anthracotheriidae (Mammalia, Bothriodontinae) from the early Miocene of Panama. J. Vertebr. Paleontol. 33, 421–433 (2013)
    Article Google Scholar
  8. Rincon, A. F., Bloch, J. I., Macfadden, B. J. & Jaramillo, C. A. New early Miocene protoceratids (Mammalia, Artiodactyla) from Panama. J. Verteb. Paleontol . http://dx.doi.org/10.1080/02724634.2015.970688 (2015)
  9. Wood, A. R. & Ridgwell, N. M. The first Central American chalicothere (Mammalia, Perissodactyla) and the paleobiogeographic implications for small-bodied schizotheriines. J. Vertebr. Paleontol . 35, e923893 (2015)
    Article Google Scholar
  10. MacFadden, B. J. et al. Temporal calibration and biochronology of the Centenario Fauna, early Miocene of Panama. J. Geol. 122, 113–135 (2014)
    Article ADS CAS Google Scholar
  11. Kirby, M. X., Jones, D. S. & MacFadden, B. J. Lower Miocene stratigraphy along the Panama Canal and its bearing on the Central American Peninsula. PLoS One 3, e2791 (2008)
    Article ADS Google Scholar
  12. Woodburne, M. O. The Great American Biotic Interchange: dispersals, tectonics, climate, sea level and holding pens. J. Mamm. Evol. 17, 245–264 (2010)
    Article Google Scholar
  13. Albright, L. B., III et al. Revised chronostratigraphy and biostratigraphy of the John Day Formation (Turtle Cove and Kimberly Members), Oregon, with implications for updated calibration of the Arikareean North American land mammal age. J. Geol. 116, 211–237 (2008)
    Article ADS Google Scholar
  14. Tedford, R. H. et al. in Late Cretaceous and Cenozoic Mammals of North America: Biostratigraphy and Geochronology 169–231 (Columbia Univ. Press, 2004)
  15. MacFadden, B. J. Chronology of Cenozoic primate localities in South America. J. Hum. Evol. 19, 7–21 (1990)
    Article Google Scholar
  16. Bond, M. et al. Eocene primates of South America and the African origins of New World monkeys. Nature 520, 538–541 (2015)
    Article ADS Google Scholar
  17. Kay, R. F. New World monkey origins. Science 347, 1068–1069 (2015)
    Article ADS CAS Google Scholar
  18. Jameson Kiesling, N. M., Yi, S. V., Xu, K., Gianluca Sperone, F. & Wildman, D. E. The tempo and mode of New World monkey evolution and biogeography in the context of phylogenomic analysis. Mol. Phylogenet. Evol. 82, 386–399 (2015)
    Article Google Scholar
  19. Houle, A. The origin of platyrrhines: an evaluation of the Antarctic scenario and the floating island model. Am. J. Phys. Anthropol. 109, 541–559 (1999)
    Article CAS Google Scholar
  20. Springer, M. S. et al. Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS ONE 7, e49521 (2012)
    Article ADS CAS Google Scholar
  21. Perelman, P. et al. A molecular phylogeny of living primates. PLoS Genet. 7, e1001342 (2011)
    Article CAS Google Scholar
  22. Cooke, S. B., Rosenberger, A. L. & Turvey, S. An extinct monkey from Haiti and the origins of the Greater Antillean primates. Proc. Natl Acad. Sci. USA 108, 2699–2704 (2011)
    Article ADS CAS Google Scholar
  23. Rosenberger, A. L. Platyrrhines, PAUP, parallelism, and the Long Lineage Hypothesis: a reply to Kay et al. (2008). J. Hum. Evol. 59, 214–217 (2010)
  24. MacPhee, R. D., Iturralde-Vinent, M. A. & Gaffney, E. S. Domo de Zaza, an early Miocene vertebrate locality in south-central Cuba, with notes on the tectonic evolution of Puerto Rico and the Mona Passage. Am. Mus. Novit. 3394, 1–42 (2003)
    Article Google Scholar
  25. Dunn, R. E. et al. A new chronology for middle Eocene–early Miocene South American Land Mammal Ages. Geol. Soc. Am. Bull. 125, 539–555 (2013)
    Article ADS Google Scholar
  26. Rosenberger, A., Tejedor, M., Cooke, S. & Pekar, S. in South American Primates Developments in Primatology: Progress and Prospects (eds Garber, P. A., Estrada, A., Bicca-Marques, J. C., Heymann, E. W. & Strier, K. B. ) Ch. 4, 69–113 (Springer, 2009)
    Article Google Scholar
  27. Jaramillo, C. et al. Palynological Record of the Last 20 Million Years in Panama. Ch. 8, 134–251 (Missouri Botanical Garden Press, 2014)
    Google Scholar
  28. Rooney, T. O., Franceschi, P. & Hall, C. M. Water-saturated magmas in the Panama Canal region: a precursor to adakite-like magma generation? Contrib. Mineral. Petrol. 161, 373–388 (2011)
    Article ADS CAS Google Scholar
  29. Black, L. P. et al. The application of SHRIMP to Phanerozoic geochronology; a critical appraisal of four zircon standards. Chem. Geol. 200, 171–188 (2003)
    Article ADS CAS Google Scholar
  30. Montes, C. et al. Arc-continent collision and orocline formation: closing of the Central American seaway. J. Geophys. Res. 117, B4 (2012)
    Article Google Scholar

Download references

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

Authors and Affiliations

  1. Florida Museum of Natural History, University of Florida, Gainesville, 32611-7800, Florida, USA
    Jonathan I. Bloch, Emily D. Woodruff, Aaron R. Wood, Aldo F. Rincon, Arianna R. Harrington, Nathan A. Jud, Douglas S. Jones & Bruce J. MacFadden
  2. Department of Biology, University of Florida, Gainesville, 32611-7800, Florida, USA
    Emily D. Woodruff & Arianna R. Harrington
  3. Department of Geological and Atmospheric Sciences, Iowa State University, Ames, 50011-1027, Iowa, USA
    Aaron R. Wood
  4. Department of Geological Sciences, University of Florida, Gainesville, 32611-7800, Florida, USA
    Aldo F. Rincon & David A. Foster
  5. Department of Evolutionary Anthropology, Duke University, Durham, 27708-9976, North Carolina, USA
    Arianna R. Harrington
  6. New Mexico Museum of Natural History and Science, Albuquerque, 87104, New Mexico, USA
    Gary S. Morgan
  7. Geociencias, Universidad de los Andes, Calle 1A # 18A-10, Edificio IP, 111711, Bogotá DC, Colombia
    Camilo Montes
  8. Smithsonian Tropical Research Institute, Balboa, Box 0843-03092, Ancon, Republic of Panama
    Carlos A. Jaramillo

Authors

  1. Jonathan I. Bloch
  2. Emily D. Woodruff
  3. Aaron R. Wood
  4. Aldo F. Rincon
  5. Arianna R. Harrington
  6. Gary S. Morgan
  7. David A. Foster
  8. Camilo Montes
  9. Carlos A. Jaramillo
  10. Nathan A. Jud
  11. Douglas S. Jones
  12. Bruce J. MacFadden

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 toJonathan I. Bloch.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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.

a–d, 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, e–g): 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.

a–g, 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.

a–k, 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.

a–i, 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 (download PDF )

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 (download PDF )

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 (download ZIP )

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 (download ZIP )

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)

PowerPoint slides

Rights and permissions

About this article

Cite this article

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

Download citation