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Palaeoproteomics resolves sloth relationships

Nature Ecology & Evolution volume 3, pages 1121–1130 (2019)Cite this article

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Abstract

The living tree sloths Choloepus and Bradypus are the only remaining members of Folivora, a major xenarthran radiation that occupied a wide range of habitats in many parts of the western hemisphere during the Cenozoic, including both continents and the West Indies. Ancient DNA evidence has played only a minor role in folivoran systematics, as most sloths lived in places not conducive to genomic preservation. Here we utilize collagen sequence information, both separately and in combination with published mitochondrial DNA evidence, to assess the relationships of tree sloths and their extinct relatives. Results from phylogenetic analysis of these datasets differ substantially from morphology-based concepts: Choloepus groups with Mylodontidae, not Megalonychidae; Bradypus and Megalonyx pair together as megatherioids, while monophyletic Antillean sloths may be sister to all other folivorans. Divergence estimates are consistent with fossil evidence for mid-Cenozoic presence of sloths in the West Indies and an early Miocene radiation in South America.

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Fig. 1: Phylogenetic relationships among major folivoran taxa based on morphological evidence, with existence of unallocated taxa acknowledged.
Fig. 2: Geographical locations of sequenced samples.
Fig. 3: Fifty percent majority rule consensus tree from Bayesian analysis of the proteomic data without temporal information, as performed in MrBayes.
Fig. 4: Time-scaled maximum clade credibility tree from BEAST analysis of 24 extant and extinct xenarthran collagen sequences plus published mitochondrial genomes.

Data availability

Mass spectrometry proteomics data have been deposited with the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD012859. Collagen sequences are available on the Uniprot website (https://www.uniprot.org/); the complete list can be found in Supplementary Table 5. Phylogenetic datasets have been deposited at DataDryad (https://doi.org/10.5061/dryad.7dd64gs).

Change history

  • 14 June 2019

    An old version of the Supplementary Information was originally uploaded. This has now been replaced with the correct version.

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Acknowledgements

We thank the curatorial staffs of the following museums and private collections for permission to sample specimens in their care: AMNH-M, American Museum of Natural History (Mammalogy), New York, USA; AMNH-P, American Museum of Natural History (Paleontology), New York, USA; CIV, Iota Quatro faunal collection, courtesy of Lazaro Vinola; El Trebol faunal collection, Bariloche, Argentina; FR, Forest Reserve (Trinidad) faunal collection currently housed in Department of Mammalogy, AMNH, New York, USA; IANIGLA-PV, Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales, CCT-CONICET-Mendoza, Mendoza, Argentina; MACN-PV, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (Sección Paleovertebrados), Buenos Aires, Argentina; MAPBAR, Museo de la Asociación Paleontológica Bariloche (APB), prov. Río Negro, Argentina; MMP, Museo Municipal de Ciencias Naturales ‘Lorenzo Scaglia’ Mar del Plata, prov. Buenos Aires, Argentina; MNHN SAO, Muséum national d’Histoire naturelle, Paris, France; MPS, Museo Paleontológico ‘Fray Manuel de Torres’, San Pedro, prov. Buenos Aires, Argentina; MUSM, Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos, Lima, Peru; NYSM VP, New York State Museum (Vertebrate Paleontology), Albany, USA; RM, Cuban faunal collection currently housed in Department of Mammalogy, AMNH, New York, USA; UF, University of Florida, Natural History Museum of Florida (Vertebrate Paleontology), Gainesville, USA; UMAG ah, Instituto de La Patagonia, Universidad de Magallanes, Punta Arenas, Chile; USNM, United States National Museum of Natural History (Paleobiology), Washington DC, USA. Samples of specimens housed in Argentinian collections were sampled before 2009. S.P. would like to thank B. Demarchi for useful discussion and support. The authors thank the National Science Foundation for grants (No. OPP 0636639 to R.D.E.M. and No. DEB 1547414 to R.D.E.M., M.C. and K.P.).

Author information

Author notes

  1. These authors contributed equally: S. Presslee, G. J. Slater.

Authors and Affiliations

  1. Department of Archaeology and BioArCh, University of York, Heslington, UK

    Samantha Presslee

  2. Department of Mammalogy, American Museum of Natural History, New York, NY, USA

    Samantha Presslee & Ross D. E. MacPhee

  3. Paleoproteomics Group, Natural History Museum of Denmark and University of Copenhagen, Copenhagen, Denmark

    Samantha Presslee, Meaghan Mackie & Matthew Collins

  4. Department of the Geophysical Sciences, University of Chicago, Chicago, IL, USA

    Graham J. Slater

  5. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales, CCT-CONICET-Mendoza, Mendoza, Argentina

    François Pujos & Analía M. Forasiepi

  6. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK

    Roman Fischer

  7. Chait Laboratory and National Resource for the Mass Spectrometric Analysis of Biological Macromolecules, The Rockefeller University, New York, NY, USA

    Kelly Molloy & Brian T. Chait

  8. Novo Nordisk Foundation Center for Protein Research, Copenhagen, Denmark

    Meaghan Mackie & Jesper V. Olsen

  9. Sección Paleovertebrados, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina

    Alejandro Kramarz

  10. Museo Municipal de Ciencias Naturales ‘Lorenzo Scaglia’, Mar del Plata, Argentina

    Matías Taglioretti & Fernando Scaglia

  11. Instituto de Investigaciones en Diversidad Cultural y Procesos de Cambio, CONICET and Universidad Nacional de Río Negro, Bariloche, Argentina

    Maximiliano Lezcano & José Luis Lanata

  12. Keck-CCAMS Group, Earth System Science Department, University of California, Irvine, Irvine, CA, USA

    John Southon

  13. New York State Museum, Albany, NY, USA

    Robert Feranec

  14. Florida Museum of Natural History, University of Florida, Gainesville, FL, USA

    Jonathan Bloch

  15. Museo de la Patagonia ‘F. P. Moreno’, Bariloche, Argentina

    Adam Hajduk

  16. Centro de Estudios del Hombre Austral, Instituto de la Patagonia, Universidad de Magallanes, Punta Arenas, Chile

    Fabiana M. Martin

  17. BioGeoCiencias Lab, Facultad de Ciencias y Filosofía/CIDIS, Universidad Peruana Cayetano Heredia, Lima, Peru

    Rodolfo Salas Gismondi

  18. CONICET and División Paleontología de Vertebrados, Museo de La Plata. Facultad de Ciencias Naturales, Universidad Nacional de La Plata, La Plata, Argentina

    Marcelo Reguero

  19. Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements, Muséum national d’Histoire naturelle, Paris, France

    Christian de Muizon

  20. Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

    Alex Greenwood

  21. Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany

    Alex Greenwood

  22. Department of Chemistry, University of York, Heslington, UK

    Kirsty Penkman

  23. McDonald Institute for Archaeological Research, University of Cambridge, Cambridge, UK

    Matthew Collins

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  1. Samantha Presslee
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Contributions

R.D.E.M., M.C. and S.P. conceived the project. S.P. undertook AAR, proteomic analysis and concatenated collagen sequences, with laboratory and technical assistance from R.F., J.V.O., K.M., M.M., M.C., K.P. and B.T.C. G.J.S. conducted phylogenetic analyses. F.P. and A.M.F. supplied palaeontological information. A.K., M.T., F.S., M.L., A.H., R.F., J.B., J.L.L., F.M.M., R.S.G., M.R., A.G., C.d.M. and J.S. supplied fossil samples, locality information, dating, species identifications and commentary on the manuscript. R.D.E.M., S.P. and G.J.S. wrote the manuscript, with input from all authors.

Corresponding author

Correspondence to Ross D. E. MacPhee.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary analyses, Supplementary References, Supplementary Figs. 1–6 and legends for Supplementary Tables 1–5

Reporting Summary

Supplementary Table 1

Information on all samples investigated for this study

Supplementary Table 2

Radiocarbon dates for specimens successfully screened for MS/MS

Supplementary Table 3

Marginal Likelihoods estimated for three clock models for proteomic data alone and proteomic + genomic data using the path sampling algorithm in BEAST 2.5.1

Supplementary Table 4

Detected amino acid differences between Megatherium sequence reported in ref. 15 (denoted by B) and the sequence concatenated in this study (TS)

Supplementary Table 5

Accession numbers of collagen sequences used in this study

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Presslee, S., Slater, G.J., Pujos, F. et al. Palaeoproteomics resolves sloth relationships. Nat Ecol Evol 3, 1121–1130 (2019). https://doi.org/10.1038/s41559-019-0909-z

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