Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution
Zhe-Xi Luo a, Stephen M. Gatesy b, Farish A. Jenkins, Jr. c,d,1, William W. Amaral c,d,2, and Neil H. Shubin a,3
aDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
bDepartment of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912;
cDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
dMuseum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Contributed by Neil H. Shubin, October 5, 2015 (sent for review July 29, 2015; reviewed by Guillermo W. Rougier and Timothy B. Rowe)
Bi et al. 2014
Significance
The origins and earliest evolution of mammals can be deciphered by studying Late Triassic fossil relatives of modern mammals. The computed tomography study of Haramiyavia from the Late Triassic has revealed new information about the skull evolution and dental function in the forerunners of mammals. Haramiyavia had a unique way of chewing. Its teeth of multiple cusp-rows were adapted to omnivory or herbivory and are distinctive from the teeth of other early mammal relatives that are presumed to be insectivorous. On the mammal family tree Haramiyavia occupies a position crucial for dating the initial appearance of the major mammalian groups. Our reanalysis affirms that the earliest diversification of mammals occurred in the Jurassic.
Abstract
As one of the earliest-known mammaliaforms, Haramiyavia clemmenseni from the Rhaetic (Late Triassic) of East Greenland has held an important place in understanding the timing of the earliest radiation of the group. Reanalysis of the type specimen using high-resolution computed tomography (CT) has revealed new details, such as the presence of the dentary condyle of the mammalian jaw hinge and the postdentary trough for mandibular attachment of the middle ear—a transitional condition of the predecessors to crown Mammalia. Our tests of competing phylogenetic hypotheses with these new data show that Late Triassic haramiyids are a separate clade from multituberculate mammals and are excluded from the Mammalia. Consequently, hypotheses of a Late Triassic diversification of the Mammalia that depend on multituberculate affinities of haramiyidans are rejected. Scanning electron microscopy study of tooth-wear facets and kinematic functional simulation of occlusion with virtual 3D models from CT scans confirm that Haramiyavia had a major orthal occlusion with the tallest lingual cusp of the lower molars occluding into the lingual embrasure of the upper molars, followed by a short palinal movement along the cusp rows alternating between upper and lower molars. This movement differs from the minimal orthal but extensive palinal occlusal movement of multituberculate mammals, which previously were regarded as relatives of haramiyidans. The disparity of tooth morphology and the diversity of dental functions of haramiyids and their contemporary mammaliaforms suggest that dietary diversification is a major factor in the earliest mammaliaform evolution.
mammaliaform haramiyid occlusion Rhaetic
Footnotes
1Deceased November 11, 2012.
2Deceased March 20, 2015.
3To whom correspondence should be addressed. Email: nshubin{at}uchicago.edu.
Author contributions: Z.-X.L., S.M.G., F.A.J., W.W.A., and N.H.S. designed research; Z.-X.L., S.M.G., F.A.J., W.W.A., and N.H.S. performed research; S.M.G., F.A.J., W.W.A., and N.H.S. performed fieldwork; Z.-X.L. performed the digital analyses; Z.-X.L. contributed new reagents/analytic tools; Z.-X.L., S.M.G., and N.H.S. analyzed data; and Z.-X.L., S.M.G., and N.H.S. wrote the paper.
Reviewers: G.W.R., University of Louisville; and T.B.R., University of Texas.
The authors declare no conflict of interest.
Data deposition: The data reported in this paper have been deposited in Morphobank.org (accession no. Project 2292).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1519387112/-/DCSupplemental.
Freely available online through the PNAS open access option.
FREE PDF GRATIS: PNAS
