Varanopid from the Carboniferous of Nova Scotia reveals evidence of parental care in amniotes

Abstract

Here we report on a fossil synapsid, Dendromaia unamakiensis gen. et sp. nov., from the Carboniferous period of Nova Scotia that displays evidence of parental care—approximately 40 million years earlier than the previous earliest record based on a varanopid from the Guadalupian (middle Permian) period of South Africa. The specimen, consisting of an adult and associated conspecific juvenile, is also identified as a varanopid suggesting parental care is more deeply rooted within this clade and evolved very close to the origin of Synapsida and Amniota in general. This specimen adds to growing evidence that parental care was more widespread among Palaeozoic synapsids than previously thought and further provides data permitting the identification of potential ontogeny-dependent traits within varanopids, the implications of which impact recent competing hypotheses of the phylogenetic affinities of the group.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Locality and horizon information for D. unamakiensis gen. et sp. nov. (NSM017GF020.001).
Fig. 2: Photographs of D. unamakiensis gen. et sp. nov. (NSM017GF020.001).
Fig. 3: Illustrations of D. unamakiensis gen. et sp. nov. (NSM017GF020.001).
Fig. 4: Photographs of the small individual of D. unamakiensis gen. et sp. nov. (NSM017GF020.001).
Fig. 5: Time-calibrated strict consensus tree from the parsimony-based phylogenetic analysis including D. unamakiensis gen. et sp. nov. (NSM017GF020.001).

Data availability

Specimen NSM017GF020.001 is accessioned in the Nova Scotia Museum. See Supplementary Information and Dataset for character list and character–taxon matrix used in the currently analyses.

References

  1. 1.

    Drent, R. H. & Daan, S. The prudent parent: energetic adjustments in avian breeding. Ardea 68, 225–252 (1980).

  2. 2.

    Smiseth, P. T., Kölliker, M. & Royle, N. J. in The Evolution of Parental Care (eds Royle, N. J. et al.) 1–14 (Oxford Univ. Press, 2012).

  3. 3.

    Jasinoski, S. C. & Abdala, F. Aggregations and parental care in the Early Triassic basal cynodonts Galesaurus planiceps and Thrinaxodon liorhinus. PeerJ 5, e2875 (2017).

  4. 4.

    Meng, Q., Liu, J., Varricchio, D. J., Huang, T. & Gao, C. Parental care in an ornithischian dinosaur. Nature 431, 145–146 (2004).

  5. 5.

    Varricchio, D. J., Martin, A. J. & Katsura, Y. First trace and body fossil of a burrowing, denning dinosaur. Proc. R. Soc. Lond. B 274, 1361–1368 (2007).

  6. 6.

    Botha-Brink, J. & Modesto, S. P. A mixed-age classed ‘pelycosaur’ aggregation from South Africa: earliest evidence of parental care in amniotes? Proc. R. Soc. Lond. B 274, 2829–2834 (2007).

  7. 7.

    Lü, J., Kobayashi, Y., Deeming, D. C. & Liu, Y. Post-natal parental care in a Cretaceous diapsid from northeastern China. Geosci. J. 19, 273–280 (2015).

  8. 8.

    Aleksiuk, M. Cold-induced aggregative behavior in the Red-Sided Garter Snake (Thamnophis sirtalis parietalis). Herpetologica 33, 98–101 (1977).

  9. 9.

    Rivas, J. A. & Burghardt, G. M. Snake mating systems, behavior, and evolution: the revisionary implications of recent findings. J. Comp. Psychol. 119, 447–454 (2005).

  10. 10.

    Spindler, F. et al. First arboreal ‘pelycosaurs’ (Synapsida: Varanopidae) from the early Permian Chemnitz Fossil Lagerstätte, SE-Germany, with a review of varanopid phylogeny. Paläont. Zeit. 92, 315–364 (2018).

  11. 11.

    Reisz, R. R. & Dilkes, D. W. Archaeovenator hamiltonensis, a new varanopid (Synapsida: Eupelycosauria) from the Upper Carboniferous of Kansas. Can. J. Earth Sci. 40, 667–678 (2003).

  12. 12.

    Haeckel, E. Generelle Morphologie der Organismen (G. Reimer, 1866).

  13. 13.

    Romer, A. S. & Price, L. I. Review of the Pelycosauria. Geol. Soc. Am. Spec. Pap. 28, 1–538 (1940).

  14. 14.

    Allen, J. P., Fielding, C. R., Gibling, M. R. & Rygel, M. C. Recognizing products of palaeoclimate fluctuation in the fluvial stratigraphic record: an example from the Pennsylvanian to Lower Permian of Cape Breton Island, Nova Scotia. Sedimentology 61, 1332–1382 (2014).

  15. 15.

    Berman, D. S. & Reisz, R. R. Restudy of Mycterosaurus longiceps (Reptilia, Pelycosauria) from the Lower Permian of Texas. Ann. Carn. Mus. 51, 423–453 (1982).

  16. 16.

    Botha-Brink, J. & Modesto, S. P. Anatomy and relationships of the Middle Permian varanopid Heleosaurus scholtzi based on a social aggregation from the Karoo Basin of South Africa. J. Vert. Paleontol. 29, 389–400 (2009).

  17. 17.

    Reisz, R. R. & Modesto, S. P. Heleosaurus scholtzi from the Permian of South Africa: a varanopid synapsid, not a diapsid reptile. J. Vert. Paleontol. 27, 734–739 (2007).

  18. 18.

    Carroll, R. L. in Athlon: Essays on Paleontology in Honour of Loris Shano Russell (ed. Churcher, C. S.) 58–79 (Misc. Publ. R. Ont. Mus., 1976).

  19. 19.

    Anderson, J. S. & Reisz, R. R. Pyozia mesenensis, a new, small varanopid (Synapsida, Eupelycosauria) from Russia: “pelycosaur” diversity in the Middle Permian. J. Vert. Paleontol. 24, 173–179 (2004).

  20. 20.

    Davies, N. S. & Gibling, M. R. Evolution of fixed-channel alluvial plains in response to Carboniferous vegetation. Nat. Geosci. 4, 629–633 (2011).

  21. 21.

    Gibling, M. R. & Davies, N. S. Palaeozoic landscapes shaped by plant evolution. Nat. Geosci. 5, 99–105 (2012).

  22. 22.

    Ielpi, A., Gibling, M. R., Bashforth, A. R. & Dennar, C. I. Impact of vegetation on Early Pennsylvanian fluvial channels: insights from the Joggins Formation of Atlantic Canada. J. Sediment. Res. 85, 999–1018 (2015).

  23. 23.

    Steyer, J. S. Ontogeny and phylogeny in temnospondyls: a new method of analysis. Zool. J. Linn. Soc. 130, 449–467 (2000).

  24. 24.

    Tsuihiji, T. et al. Cranial osteology of juvenile specimens of Tarbosaurus bataar (Theropoda, Tyrannosauridae) from the Nemegt Formation (Upper Cretaceous of Bugin Tzav, Mongolia). J. Vert. Paleontol. 31, 497–517 (2011).

  25. 25.

    Campione, N. E., Brink, K. S., Freedman, E. A., McGarrity, C. T. & Evans, D. C. ‘Glishades ericksoni’, an indeterminate juvenile hadrosaurid from the Two Medicine Formation of Montana: implications for hadrosauroid diversity in the latest Cretaceous (Campanian-Maastricthian) of western North America. Palaeobio. Palaeoenv. 93, 65–75 (2013).

  26. 26.

    Tsai, C. H. & Fordyce, R. E. Juvenile morphology in baleen whale phylogeny. D. Naturwissen. 101, 765–769 (2014).

  27. 27.

    Maddin, H. C., Evans, D. C. & Reisz, R. R. An Early Permian varanodontine varanopid (Synapsida: Eupelycosauria) from the Richards Spur Locality, Oklahoma. J. Vert. Paleontol. 26, 957–966 (2006).

  28. 28.

    Ford, D. P. & Benson, R. A redescription of Orovenator mayorum (Sauropsida, Diapsida) using high-resolution μCT, and the consequences for early amniote phylogeny. Pap. Palaeontol. 5, 197–239 (2019).

  29. 29.

    Ford, D. P. & Benson, R. B. J. The phylogeny of early amniotes and the affinities of Parareptilia and Varanopidae. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-019-1047-3 (2019).

  30. 30.

    Brocklehurst, N. & Fröbisch, J. A reexamination of Milosaurus mccordi, and the evolution of large body size in Carboniferous synapsids. J. Vert. Paleontol. 38, e1508026 (2018).

  31. 31.

    Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4.0b8 (Sinauer Associates, 2002).

  32. 32.

    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

  33. 33.

    Brocklehurst, N., Reisz, R. R., Fernandez, V. & Fröbisch, J. A re-description of ‘Mycterosaurus’ smithae, an Early Permian eothyridid, and its impact on the phylogeny of pelycosaurian-grade synapsids. PLoS ONE 11, e0156810 (2016).

  34. 34.

    Fracasso, M. A. Age of the Permo-Carboniferous Cutler Formation vertebrate fauna from El Cobre Canyon, New Mexico. J. Paleontol. 54, 1237–1244 (1980).

  35. 35.

    Langston, W. Permian amphibian from New Mexico. Univ. Calif. Publ. Geol. Sci. 29, 349–416 (1953).

  36. 36.

    Vaughn, P. P. The age and locality of the Late Paleozoic vertebrates from El Cobre Canyon, Rio Arriba County, New Mexico. J. Paleontol. 37, 283–286 (1963).

  37. 37.

    Langston, W. & Reisz, R. R. Aerosaurus wellesi, new species, a varanopseid mammal-like reptile (Synapsida: Pelycosauria) from the Lower Permian of New Mexico. J. Vert. Paleontol. 1, 73–96 (1981).

Download references

Acknowledgements

We thank T. Fedak, M. Grey, K. Ogden and staff at the Nova Scotia Museum for facilitating the loan of this material. We also thank S. W. McKeane and Provincial staff for assistance with permits. We thank J. Calder, D. Scott, J. Pardo, B. Gee, R. Hook, S. Modesto and R. Reisz for discussions. We thank D. Gray for assistance in the field. We acknowledge our field site is located in Mi’kma’ki territory of the Mi’kmaq people. Funding was provided in part by the Natural Sciences and Engineering Research Council of Canada discovery grant (no. 04633 to H.C.M.).

Author information

H.C.M. was principal investigator. B.H. discovered the specimen. A.M. and H.C.M. prepared and illustrated the specimen. All authors contributed to discussion, preparation and writing of the manuscript.

Correspondence to Hillary C. Maddin.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Character list and Supplementary Figs. 1 and 2.

Reporting Summary

Supplementary Dataset

Character–taxon matrix.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maddin, H.C., Mann, A. & Hebert, B. Varanopid from the Carboniferous of Nova Scotia reveals evidence of parental care in amniotes. Nat Ecol Evol 4, 50–56 (2020). https://doi.org/10.1038/s41559-019-1030-z

Download citation

Further reading