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Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity

Nature volume 581, pages 421–427 (2020)Cite this article

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Abstract

The fossil record of mammaliaforms (mammals and their closest relatives) of the Mesozoic era from the southern supercontinent Gondwana is far less extensive than that from its northern counterpart, Laurasia1,2. Among Mesozoic mammaliaforms, Gondwanatheria is one of the most poorly known clades, previously represented by only a single cranium and isolated jaws and teeth1,2,3,4,5. As a result, the anatomy, palaeobiology and phylogenetic relationships of gondwanatherians remain unclear. Here we report the discovery of an articulated and very well-preserved skeleton of a gondwanatherian of the latest age (72.1–66 million years ago) of the Cretaceous period from Madagascar that we assign to a new genus and species, Adalatherium hui. To our knowledge, the specimen is the most complete skeleton of a Gondwanan Mesozoic mammaliaform that has been found, and includes the only postcranial material and ascending ramus of the dentary known for any gondwanatherian. A phylogenetic analysis including the new taxon recovers Gondwanatheria as the sister group to Multituberculata. The skeleton, which represents one of the largest of the Gondwanan Mesozoic mammaliaforms, is particularly notable for exhibiting many unique features in combination with features that are convergent on those of therian mammals. This uniqueness is consistent with a lineage history for A. hui of isolation on Madagascar for more than 20 million years.

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Fig. 1: Skull and postcranial skeleton of A. hui holotype (UA 9030).
Fig. 2: Cranium, lower jaw and dentition of A. hui holotype (UA 9030).
Fig. 3: Skeleton of A. hui holotype (UA 9030).
Fig. 4: Key stages in plate tectonic history of Madagascar.

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Data availability

The holotype of A. hui is catalogued into the University of Antananarivo collections. Graphics and phylogenetics data are provided in the Supplementary Information. The Life Science Identifiers (LSID) for the new family, genus and species are registered with Zoobank (http://zoobank.org) with the identifiers urn:lsid:zoobank.org:act:DA019E3D-6B27-4728-9321-A0502EA0FEC4, urn:lsid:zoobank.org:act:3DEB862B-5A3E-40A2-B939-A2B549A0AC62 and urn:lsid:zoobank.org:act:9CB87C13-10B6-4FE7-B450-BE89D4E6BD88, respectively. The data matrix for the phylogenetic analysis has been deposited in MorphoBank at http://morphobank.org/permalink/?P3411.

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Acknowledgements

We thank the Université d’Antananarivo, the Madagascar Institut pour la Conservation des Ecosystèmes Tropicaux and the villagers of the Berivotra Study Area for logistical support of fieldwork; the ministries of Mines and Higher Education of the Republic of Madagascar for permission to conduct field research; members of the 1999 field research team for their efforts; and the National Geographic Society and the National Science Foundation for funding. Full acknowledgments are provided in the Supplementary Information.

Author information

Author notes

  1. Deceased: Yaoming Hu

Authors and Affiliations

  1. Department of Earth Sciences, Denver Museum of Nature and Science, Denver, CO, USA

    David W. Krause

  2. Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA

    David W. Krause, Yaoming Hu & Joseph R. Groenke

  3. Department of Anatomy, College of Osteopathic Medicine, New York Institute of Technology, Old Westbury, NY, USA

    Simone Hoffmann

  4. Section of Mammals, Carnegie Museum of Natural History, Pittsburgh, PA, USA

    John R. Wible

  5. Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, USA

    Guillermo W. Rougier

  6. Department of Anthropology, University of Texas at Austin, Austin, TX, USA

    E. Christopher Kirk

  7. Jackson School Museum of Earth History, University of Texas at Austin, Austin, TX, USA

    E. Christopher Kirk

  8. Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, OH, USA

    Joseph R. Groenke

  9. Geology Department, Macalester College, St Paul, MN, USA

    Raymond R. Rogers

  10. Department of Anthropology, Stony Brook University, Stony Brook, NY, USA

    James B. Rossie

  11. Institut für Geowissenschaften, Universität Bonn, Bonn, Germany

    Julia A. Schultz & Wighart von Koenigswald

  12. School of Biological Sciences, Monash University, Clayton, Victoria, Australia

    Alistair R. Evans

  13. Geosciences, Museums Victoria, Melbourne, Victoria, Australia

    Alistair R. Evans

  14. Département de Sciences de la Terre et de l’Environnement, Université d’Antananarivo, Antananarivo, Madagascar

    Lydia J. Rahantarisoa

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Contributions

D.W.K., S.H. and Y.H. conceived the project; J.R.G. and S.H. contributed to μCT digital preparation of the specimen; R.R.R. and L.J.R. provided geological data and interpretation; E.C.K., D.W.K. and S.H. developed the body mass estimates; D.W.K., S.H., Y.H., J.R.W., J.B.R, G.W.R., J.R.G., J.A.S., A.R.E., E.C.K. and W.v.K. conducted laboratory work on the fossil and contributed to descriptions and comparisons; S.H., D.W.K., J.R.W. and G.W.R. contributed to the phylogenetic analysis; D.W.K. wrote the manuscript, with contributions and/or editing from all authors.

Corresponding author

Correspondence to David W. Krause.

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The authors declare no competing interests.

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Peer review information Nature thanks Jin Meng and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Photographs of the skeleton of A. hui holotype (UA 9030).

a, b, ‘Top’ (a) and ‘bottom’ (b) views, as preserved. The left and right sides are indicated as (l) and (r), respectively. as, astragalus; at, atlas; av, anticlinal vertebra; ax, axis; C, cervical vertebra; ca, calcaneus; Ca, caudal vertebra; cap, capitate; CC, costal cartilage; cl, clavicle; cor, coracoid; cu, cuboid; dpp, distal pedal phalanx; ent, entocuneiform; ep, epipubis; fe, femur; fi, fibula; ha, hamate; hu, humerus; i, lower incisor; ID, distal upper incisor; IM, medial upper incisor; imp, intermediate manual phalanx; ipp, intermediate pedal phalanx; L, lumbar vertebra; lu, lunate; m, mandible; mc, metacarpal; mt, metatarsal; na, navicular; osc, os calcaris; pc1, lower first postcanine tooth; PC1, upper first postcanine tooth; pe, pelvis; pfi, parafibula; pi, pisiform; pmp, proximal manual phalanx; ppp, proximal pedal phalanx; R, rib; ra, radius; sc, scapula; sca, scaphoid; stb, sternebra; T, thoracic vertebra; ti, tibia; tr, triquetrum; ul, ulna.

Extended Data Fig. 2 Bivariate plots of body mass estimates for A. hui.

a, Relationship between cranial length and body mass in 423 extant mammals, plus estimated body mass in the gondwanatherians A. hui and Vintana sertichi. b, Relationship between cranial width and body mass in 423 extant mammals, plus the estimated body mass in A. hui and V. sertichi. c, Relationship between cranial size and body mass in 423 extant mammals, plus the estimated body mass in A. hui and V. sertichi. d, Relationship between humeral length and body mass in 187 extant therian mammals, plus the estimated body mass in A. hui. e, Relationship between femoral length and body mass in 184 extant species of therian mammal, plus the estimated body mass in A. hui. f, Relationship between stylopodial diaphyseal circumference and body mass as calculated for a sample of 245 tetrapod species45 (data points shown for mammals only, n = 200), plus the estimated body mass in A. hui. Regression lines in a–e are from ordinary least squares regressions, whereas the regression line shown in f is from a phylogenetic generalized least squares regression. Measurement data, methods and references are provided in the Supplementary Information.

Extended Data Fig. 3 Cranium of A. hui holotype (UA 9030).

a–e, Photographs of external surfaces of cranium in right lateral (a), left lateral (b), dorsal (c), ventral (d) and anterior (e) views. a'–e', Labelled μCT images of cranium in the same views as in a–e, respectively. f, Labelled μCT image of medial view of right side of nasal cavity. aC, alveolus for upper canine; as, alisphenoid; eo, exoccipital; fr, frontal; ID, distal upper incisor; IM, mesial upper incisor; ju, jugal; la, lacrimal; mx, maxilla; na, nasal; os/ps, orbitosphenoid/presphenoid complex; PC, upper postcanine tooth; pe, petrosal; pmx, premaxilla; pt, pterygoid; smx, septomaxilla; sq, squamosal; v, vomer.

Extended Data Fig. 4 Inner ear of A. hui holotype (UA 9030).

a, Ventral view of reconstructed cranium, with petrosal fragment bounded by red line enlarged in a'. b–e, Reconstructed cochlear canal in dorsomedial (b), ventrolateral (c) and posteroventromedial (d, e) views, with the view in d being slightly more posterior and the view in e slightly more medial. In e, only the medial aspect of cochlear canal in grey is shown, to reveal primary bony lamina and cochlear nerve foramina. Semi-transparent grey, cochlear canal; yellow, cochlear nerve; blue, secondary canal.

Extended Data Fig. 5 Lower jaw of A. hui holotype (UA 9030).

Photographs of left dentary in left column; photographs of right dentary in right column. a, b, Lateral views. c, d, Dorsal (occlusal) views. e, f, Medial views. i, lower incisor; pc, lower postcanine tooth.

Extended Data Fig. 6 Enamel microstructure of A. hui holotype (UA 9030).

a–d, Scanning electron micrographs of single postcanine tooth enamel fragment sectioned in various planes. a, Transverse section of entire enamel band from the enamel–dentine junction (EDJ) to the outer enamel surface (OES) (about 0.4-mm thick) showing single layer of radial enamel and absence of distinct layer of prismless external enamel. Prism size increases from, on average, 2.3 to 2.8 μm from the enamel–dentine junction to the outer enamel surface. Prisms close to the enamel–dentine junction are intersected by interprismatic matrix at slightly higher angles than towards the outer enamel surface. b, Transverse section showing the clear distinction between enamel prisms and interprismatic matrix. c, Radial section showing radial enamel in outer zone with prisms surrounded by interprismatic matrix and some cross-sections of prisms showing tubules. d, Radial, but slightly oblique, section showing enamel of inner zone with prisms enveloped by interprismatic matrix and presence of odontoblastic processes. In this zone, crystallites of interprismatic matrix lie almost perpendicular to those of prisms. Prisms rise from the enamel–dentine junction at angle of about 45°; this angle is reduced only slightly towards the outer enamel surface. IPM, interprismatic matrix; od, odontoblastic process; p, prism; tu, tubule.

Extended Data Fig. 7 Selected individual vertebrae of A. hui holotype (UA 9030).

Thoracic (T6 and T16), lumbar (L1 and L11) and anterior caudal (Ca8) vertebrae are depicted in anterior, dorsal, left lateral and ventral views. The left transverse process of L11 is preserved but was separated from the vertebral column during preparation and has not been CT scanned. Dotted outlines represent the shape of preserved left transverse process, and the mirrored reconstructed right transverse process.

Extended Data Fig. 8 Limb bone elements of A. hui holotype (UA 9030).

a–p, μCT images. a, b, Left humerus in anterior (a) and posterior (b) views. c, d, Left ulna in anterior (c) and lateral (d) views. e, f, Left radius in anterior (e) and lateral (f) views. g, h, Left manus in dorsal (g) and palmar ( = ventral) (h) views. i, j, Left femur in anterior (i) and posterior (j) views. k, l, Left tibia in anterior (k) and lateral (l) views. m, n, Left fibula in anterior (m) and lateral (n) views. o, p, Left pes in dorsal (o) and plantar ( = ventral) (p) views.

Extended Data Fig. 9 Pectoral and pelvic girdle elements of A. hui holotype (UA 9030).

a–d, μCT images. a, b, Left scapulacoracoid, left and right clavicle and manubrium in ‘top’ (a) and ‘bottom’ (b) views (as preserved). c, d, Left os coxa and epipubic bone in lateral (c) and medial (d) views.

Extended Data Fig. 10 Phylogenetic relationships of A. hui and selected mammaliaforms.

Strict consensus tree of 16 equally parsimonious trees (tree length = 2,315, consistency index = 0.3015 and retention index = 0.7001) derived from analysis of 84 cynodont taxa and 530 characters, with multistate characters unordered and unweighted. Bremer values are listed next to the nodes. Adalatherium is highlighted in red. Allotheria—consisting of Cifelliodon, Euharamiyida, Gondwanatheria (including Adalatherium) and Multituberculata—is highlighted in blue. Taxon and character lists, the data matrix, limitations and assumptions, phylogenetic methods and a more detailed explanation of the results are provided in the Supplementary Information.

Supplementary information

Supplementary Information

This file contains Supplementary Sections A-K – see contents pages for details.

Reporting Summary

Supplementary Table 1

Body mass (kg), cranial length (mm), cranial width (mm), and cranial size (mm) for 423 species in 23 orders of extant mammals.

Supplementary Table 2

Terrestrial and freshwater vertebrate taxa from the Upper Cretaceous (Maastrichtian) Maevarano Formation, Mahajanga Basin, Madagascar.

Video 1

Visualizations of cranium of Adalatherium hui (UA 9030) from μCT dataset, through three rotations (360°) about dorsoventral axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) grayscale values as in first rotation overlain with polygon outputs of digitally prepared (segmented) cranial elements in various colours; teeth, tooth fragments, and other unidentified fragments in grey tones; and endocast of modern plant root trace in red overlain on data in first rotation; and (3) polygon outputs as in second rotation but without grayscale data visualization.

Video 2

Visualizations of cranium of Adalatherium hui (UA 9030) from μCT dataset, through three rotations (360°) about anteroposterior axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) grayscale 387 values as in first rotation overlain with polygon outputs of digitally prepared (segmented) cranial elements in various colours; teeth, tooth fragments, and other unidentified fragments in grey tones; and endocast of modern plant root trace in red overlain on data in first rotation; and (3) polygon outputs as in second rotation but without grayscale data visualization.

Video 3

Visualizations of cranium of Adalatherium hui (UA 9030) from μCT dataset, with three rotations (360°) about mediolateral axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) grayscale values as in first rotation overlain with polygon outputs of digitally prepared (segmented) cranial elements in various colours; teeth, tooth fragments, and other unidentified fragments in grey tones; and endocast of modern plant root trace in red overlain on data in first rotation; and (3) polygon outputs as in second rotation but without grayscale data visualization.

Video 4

Visualization of right dentary of Adalatherium hui (UA9030) from μCT dataset, with three rotations (360°) about dorsoventral axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) polygon outputs of digitally prepared (segmented) portions of dataset, with bone in grey and colour visualization of teeth (incisor – green; pc (lower postcanine) 1 – yellow; pc2 – orange; pc3 – deep orange; pc4 – deep red); and (3) same visualization as in second rotation but with bone rendered transparent.

Video 5

Visualization of right dentary of Adalatherium hui (UA9030) from μCT dataset, with three rotations (360°) about anteroposterior axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) polygon outputs of digitally prepared (segmented) portions of dataset, with bone in grey and colour visualization of teeth (incisor – green; pc (lower postcanine) 1 – yellow; pc2 – orange; pc3 – deep orange; pc4 – deep red); and (3) same visualization as in second rotation but with bone rendered transparent.

Video 6

Visualization of left dentary of Adalatherium hui (UA9030) from μCT dataset, with three rotations (360°) about dorsoventral axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) polygon outputs of digitally prepared (segmented) portions of dataset, with bone in grey and colour visualization of teeth (incisor – green; pc (lower postcanine) 1 – yellow; pc2 – orange; pc3 – deep orange; pc4 – deep red); and (3) same visualization as in second rotation but with bone rendered transparent.

Video 7

Visualization of left dentary of Adalatherium hui (UA9030) from μCT dataset, with three rotations (360°) about anteroposterior axis. (1) grayscale mapping of data reconstruction showing relative density values of specimen and matrix; (2) polygon outputs of digitally prepared (segmented) portions of dataset, with bone in grey and colour visualization of teeth (incisor – green; pc (lower postcanine) 1 – yellow; pc2 – orange; pc3 – deep orange; pc4 – deep red); and (3) same visualization as in second rotation but with bone rendered transparent.

Video 8

Animation of preserved and digitally-reconstructed fragments of right upper dentition of Adalatherium hui (UA 9030) as polygon files derived from μCT dataset: (1) buccal (lateral) view (mesial to right) of dentition (light gray) as preserved, in context of premaxilla and maxilla (dark grey); (2) buccal view of dentition (light gray) only (premaxilla and maxilla removed); (3) buccal view of postcanine teeth as preserved, with first upper postcanine tooth (PC1) in yellow, PC2 in orange, and PC3–PC5 in multiple colours representing individual fragments; (4) buccal view of postcanine teeth separated from one another; (5) animation of postcanine tooth fragment reconstructions for PC3–PC5; (6) full rotation (360°) of reconstructed postcanine dentition in horizontal plane transitioning to occlusal (ventral) view (buccal to top) of PC3–PC5 in preserved state; (7) animation in occlusal view of fragment reconstructions from PC3–PC5; and (8) addition of missing fragments (dark grey) of right PC4 and PC5 by mirroring from left PC4 and PC5.

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Krause, D.W., Hoffmann, S., Hu, Y. et al. Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity. Nature 581, 421–427 (2020). https://doi.org/10.1038/s41586-020-2234-8

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