Letter | Published:

New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem

Nature volume 548, pages 326329 (17 August 2017) | Download Citation

Abstract

Stem mammaliaforms are forerunners to modern mammals1, and they achieved considerable ecomorphological diversity in their own right2. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized3,4,5,6,7,8,9,10,11,12. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics1,2,3,4,5,6, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar–pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.

  • Subscribe to Nature for full access:

    $199

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Definition, diagnosis, and origin of Mammalia. J. Vertebr. Paleontol. 8, 241–264 (1988)

  2. 2.

    Transformation and diversification in early mammal evolution. Nature 450, 1011–1019 (2007)

  3. 3.

    et al. New multituberculate-like teeth from the Middle Jurassic of England. Acta Palaeontol. Pol. 43, 581–606 (1998)

  4. 4.

    Review of the early allotherian mammals. Acta Palaeontol. Pol. 45, 317–342 (2000)

  5. 5.

    , , & Haramiyids and Triassic mammalian evolution. Nature 385, 715–718 (1997)

  6. 6.

    , , , & Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution. Proc. Natl Acad. Sci. USA 112, E7101–E7109 (2015)

  7. 7.

    et al. Mammals from the Late Jurassic Qigu Formation in the southern Junggar Basin, Xinjiang, northwest China. Palaeodiv. et Palaeoenviron. 90, 295–319 (2010)

  8. 8.

    , & The first Haramiyid (Mammalia, Allotheria) from the Jurassic of Russia. Dokl. Biol. Sci. 437, 103–106 (2011)

  9. 9.

    , , & A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500, 163–167 (2013)

  10. 10.

    , , & A new arboreal haramiyid shows the diversity of crown mammals in the Jurassic period. Nature 500, 199–202 (2013)

  11. 11.

    , , , & Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature 514, 579–584 (2014)

  12. 12.

    ., ., & Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear. J. Morphol. (2016)

  13. 13.

    et al. Micro-ornamentations on carapaces of Euestheria hingyuanensis (Crustaceaa: Spinificance) and its biostratigraphic significance. Acta Palaeontologica Sin. 53, 201–216 (2014)

  14. 14.

    et al. Mammalian evolution. Evolutionary development in basal mammaliaforms as revealed by a docodontan. Science 347, 760–764 (2015)

  15. 15.

    . et al. New gliding mammaliaforms from the Jurassic. Nature (2017)

  16. 16.

    , , , & Earliest evolution of multituberculate mammals revealed by a new Jurassic fossil. Science 341, 779–783 (2013)

  17. 17.

    Developmental patterns in Mesozoic evolution of mammal ears. Annu. Rev. Ecol. Evol. Syst. 42, 355–380 (2011)

  18. 18.

    , & Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472, 181–185 (2011)

  19. 19.

    et al. Occlusal pattern in paulchoffatiid multituberculates and the evolution of cusp morphology in mammaliamorphs with rodent-like dentitions. J. Mamm. Evol. 17, 177–192 (2010)

  20. 20.

    et al. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483, 457–460 (2012)

  21. 21.

    et al. The difficulties of identifying flying squirrels (Sciuridae: Pteromyini) in the fossil record. J. Vertebr. Paleontol. 25, 950–961 (2005)

  22. 22.

    & Gliding Mammals of the World (CSIRO Publishing, 2012)

  23. 23.

    et al. Mammalian evolution. An arboreal docodont from the Jurassic and mammaliaform ecological diversification. Science 347, 764–768 (2015)

  24. 24.

    The pollination of mid Mesozoic seed plants and the early history of long-proboscid insects. Ann. Mo. Bot. Gard. 97, 469–513 (2010)

  25. 25.

    A new approach to mammalian cranial analysis, illustrated by examples of prosimian primates. J. Morphol. 124, 167–180 (1968)

  26. 26.

    et al. The better to eat you with: functional correlates of tooth structure in bats. Funct. Ecol. 25, 839–847 (2011)

  27. 27.

    , et al. Evolution of dental replacement in mammals. Carnegie Mus. Nat. Hist. Bull. 36, 159–175 (2004)

  28. 28.

    et al. Generalized individual dental age stages for fossil and extant placental mammals. Paläontol. Zeitschr. 85, 321–339 (2011)

  29. 29.

    & The evolution of growth patterns in mammalian versus nonmammalian cynodonts. Paleobiology 42, 439–464 (2016)

  30. 30.

    The skull and dentition of two tritylodontid synapsids from the Lower Jurassic of western North America. Bull. Mus. Comp. Zool. 151, 217–268 (1986)

  31. 31.

    , & The lower jaw of Morganucodon. Zool. J. Linn. Soc. 53, 87–175 (1973)

  32. 32.

    , , & A new eutriconodont mammal and evolutionary development in early mammals. Nature 446, 288–293 (2007)

Download references

Acknowledgements

We thank A. Shinya for fossil preparation; S. Bi, S. Gatesy, L. Heaney, H.-J. Li, Z.-J. Gao, T. Martin, B. Patterson, N. Shubin, X.-T. Zheng and C.-F. Zhou for access to comparative specimens. Funding supported Q.-J.M. (Beijing Scientific Commission) and Z.-X.L. (UChicago-BSD). Full acknowledgments are provided in the Supplementary Information.

Author information

Affiliations

  1. Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, Illinois 60637, USA

    • Zhe-Xi Luo
    •  & April I. Neander
  2. Committee on Evolutionary Biology, The University of Chicago, Chicago, Illinois 60637, USA

    • Zhe-Xi Luo
    •  & David M. Grossnickle
  3. Beijing Museum of Natural History, Beijing 100050, China

    • Qing-Jin Meng
    • , Di Liu
    •  & Yu-Guang Zhang
  4. Hebei GEO University, Shijiazhuang 050031, Hebei Province, China

    • Qiang Ji

Authors

  1. Search for Zhe-Xi Luo in:

  2. Search for Qing-Jin Meng in:

  3. Search for David M. Grossnickle in:

  4. Search for Di Liu in:

  5. Search for April I. Neander in:

  6. Search for Yu-Guang Zhang in:

  7. Search for Qiang Ji in:

Contributions

Q.-J.M. and Z.-X.L. conceived the project; Q.-J.M., Y.-G.Z., D.L. and Q.J. acquired fossils and studied stratigraphy; all authors were involved in lab fossil work and interpretation; Z.-X.L. and D.M.G. did phylogenetic analyses; A.I.N. scanned and prepared graphics of fossils; Z.-X.L. composed figures; Z.-X.L., Q.-J.M. and D.M.G. led the writing, with feedback from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Zhe-Xi Luo or Qing-Jin Meng.

Reviewer Information Nature thanks G. Rougier and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Information parts A-Q.

  2. 2.

    Reporting Summary

Videos

  1. 1.

    Video 1: Analysis of tooth occlusion of Vilevolodon by animation of STL tooth models from CT scan

    Part 1: Comparison of distinctive cycle 1 versus cycle 2 of premolars and molars: cycle 1 has full contacts of molars and incisors, but no contact between P3/p4; cycle 2 has full contact of P3/p4 but minimal or no contacts of molars and incisors. Part 2: Molar cusp and basin identification, and cycle 1 of occlusal movement of M1/m1 and M2/m2 during (see Fig. S6). During occlusal cycle 2, the P3/p4 are the only teeth that can fully occlude; the dual mortar-pestle contacts of upper and lower molars do not occur. Thus, cycle 2 is not shown here in animation analysis Part 2 of the video. For better clarity, the un-erupted deciduous incisors are not shown in the video.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature23483

Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.