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LETTER

doi:10.1038/nature10591

Highly specialized mammalian skulls from the Late Cretaceous of South America Guillermo W. Rougier1, Sebastia´n Apesteguı´a2,3 & Leandro C. Gaetano3,4

Dryolestoids are an extinct mammalian group belonging to the lineage leading to modern marsupials and placentals1,2. Dryolestoids are known by teeth and jaws from the Jurassic period of North America and Europe2,3, but they thrived in South America up to the end of the Mesozoic era and survived to the beginnings of the Cenozoic2,4–7. Isolated teeth and jaws from the latest Cretaceous of South America provide mounting evidence that, at least in western Gondwana, dryolestoids developed into strongly endemic groups by the Late Cretaceous4–9. However, the lack of pre-Late Cretaceous dryolestoid remains made study of their origin and early diversification intractable. Here we describe the first mammalian remains from the early Late Cretaceous of South America, including two partial skulls and jaws of a derived dryolestoid showing dental and cranial features unknown among any other group of Mesozoic mammals, such as single-rooted molars preceded by double-rooted premolars, combined with a very long muzzle, exceedingly long canines and evidence of highly specialized masticatory musculature. On one hand, the new mammal shares derived features of dryolestoids1–3 with forms from the Jurassic of Laurasia, whereas on the other hand, it is very specialized and highlights the endemic, diverse dryolestoid fauna from the Cretaceous of South America. Our specimens include only the second mammalian skull known for the Cretaceous of Gondwana, bridging a previous 60-million-year gap in the fossil record, and document the whole cranial morphology of a dryolestoid, revealing an unsuspected morphological and ecological diversity for nontribosphenic mammals. Class Mammalia Linnaeus, 1758 Clade Cladotheria McKenna, 1975 Superorder Dryolestoidea Butler, 1939 Order Meridiolestida nov. Cronopio dentiacutus gen. et sp. nov. Etymology. Cronopio after the fictional, bizarre creatures central to many stories by Julio Corta´zar; dentiacutus, from Latin, meaning sharp, acute teeth. Holotype. MPCA 454 (Museo Provincial Carlos Ameghino, Cipolletti, Rı´o Negro Province, Argentina), an incomplete skull preserving a full upper dentition, but missing the braincase, part of the rostral roof and the lower jaws (Figs 1–4). Locality and horizon. Candeleros Formation (Cenomanian), Neuque´n Group10. The specimens come from the La Buitrera locality, Rı´o Negro Province, Argentina, that has yielded abundant skeletons of small vertebrates11,12 and dinosaurs13,14. See Supplementary Information for further data on age, systematics and morphology. Diagnosis and description. Medium-sized dryolestoid, with an extremely elongated rostrum, extended edentulous portion of the premaxilla, and orbits placed dorsally because of a tall zygoma with a deeply excavated masseteric fossa. Dental formula I2/?, C1/1, P4/31, M3/3. Cronopio is diagnosed by a very long canine, P1 separated from

P2 by an extensive diastema, and highly mesiodistally compressed molariforms. Upper and lower premolars are supported by two roots whereas the molars rest on a single labiolingually broad root. The lower jaw (Figs 1–2 and 4) possesses a masseteric process that juts out laterally forming a broad platform whereas the angular process is small and medially inflected. Cronopio differs from other South American dryolestoids like Leonardus cuspidatus4,8 in having a contact between the stylocone and paracrista, with a stylocone not as large, the presence of a distinct small parastylar hook and at least one less molar. Cronopio and other South American dryolestoids4,7,15 share the presence of a posterior premolar (P3 in Cronopio) with a small anterior cusp supported by a circular root and a distinct mesiodistal basin supported by a transverse one; this morphology has been interpreted previously either as distinct taxa4 or as deciduous teeth2,3. Cronopio and other South American dryolestoids share with all other dryolestoids a much taller labial crown height than lingual in the lower molars (the reverse in the uppers), a small talonid, a relatively transverse metacristid, and mesiodistally compressed trigonids1–3 (Figs 1–4). Cronopio’s canine is extremely long and moderately compressed buccolingually. The dryolestoid Drescheratherium from the Jurassic of Portugal16 also shows very long canines but not to the extent of Cronopio. A distinctive feature of Cronopio and several South American dryolestoids is the presence of complex penultimate and fully molarized ultimate premolars7–15. The penultimate premolar coincides with a sharp constriction of the rostrum, leaving a much lower anterior accessory cusp isolated from the moderately basined posterior half of the tooth. This unusual morphology, although with a better developed basin, served as the basis for the recognition of several Late Cretaceous taxa such as Barberenia and Quirogatherium5,6, which in light of the new evidence probably represent just the penultimate premolar position of other taxa4,5,17 described based on molars. Similarly shaped teeth are known for the mesungulatids Coloniatherium8, Mesungulatum4–6,17 and Peligrotherium7,15, although only for Peligrotherium is the position of the tooth P2 known unambiguously, indicating that this is a conspicuous feature of many South American dryolestoids. Previous studies5,17,18 have recognized two species of triconodont mammals in the Late Cretaceous Los Alamitos Formation; the morphology of the teeth referred to these species is similar to that of the anterior upper and lower premolars of Cronopio and Peligrotherium. We suggest that these putative triconodonts represent anterior premolar positions of dryolestoids (see Supplementary Information). Upper and lower molars of Cronopio (Fig. 4) are highly compressed mesiodistally and are single-rooted. The upper crowns are dominated by a paracone and a stylocone connected to the paracrista. Both, premolars and molars are arranged forming a gentle arch that curves posteriorly along the maxillary border. The simultaneous presence of single-rooted molars and double-rooted premolars is a unique feature distinguishing Cronopio from any other Mesozoic mammal. Cronopio’s skull shows a combination of primitive mammalian features and highly specialized traits. Cronopio shares with basal

1 Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, Kentucky 40202, USA. 2CEBBAD - Fundacio´n de Historia Natural ‘Fe´lix de Azara’, Universidad Maimo´nides, Hidalgo 775, Buenos Aires (1405), Argentina. 3CONICET, Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas. Av. Rivadavia 1917, C1033AAJ, Buenos Aires, Argentina. 4Departamento de Cs. Geolo´gicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabello´n II, C1428EHA, Buenos Aires, Argentina.

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Figure 1 | Cronopio dentiacutus MPCA 454 type skull and MPCA 453 right lower jaw. a–c, MPCA 454 skull in ventral (a) and dorsal views (b); labial view of the left upper dentition (c). d, e, Cronopio dentiacutus MPCA 453 right lower jaw in labial and lingual views (d) and detail of the left petrosal and basicranium (e).

mammaliaforms features such as the presence of a septomaxilla, an anterior lamina of the petrosal, a lateral flange, and all the elements of cranial circulation thought to be primitive for therians, including a fully developed stapedial system19. The snout of Cronopio is unusually long and narrow with a relatively large orbit, a small temporal area and a robust zygoma deeply excavated by a masseteric fossa. The craniodental morphology, in particular the low coronoid process and the hyperdeveloped masseteric fossa and process, indicates that Cronopio emphasized rotation of the jaws during mastication at the expense of a powerful bite20. With the exception of a fully definitive mammalian middle ear21, Cronopio shows that the major changes in skull morphology characterizing the hypothetical common ancestor of marsupials and placentals22 were not yet established in dryolestoids and that they retained not only a primitive non-tribosphenic dentition, but also a primitive braincase and ear region. Our phylogenetic analysis (Fig. 5) including a wide array of early mammals identifies Cronopio as a member of a cluster of South American dryolestoids (see Supplementary Information). Leonardus and other Cretaceous South American dryolestoids are successive sister groups reflecting the establishment of a Cretaceous endemic biota4,5. Although in the Cretaceous of Laurasia marsupial and placental (therians) relatives were major components of the fauna, they are yet to be unequivocally identified in the admittedly sparse localities of South America2,23. Depending on how some controversial fossils from

Australia and Africa are interpreted24,25, tribosphenic mammals would also be originally absent from those continents during the Jurassic and earliest Cretaceous, despite Africa–Europe contacts during the Cretaceous2,26. However, an Early Cretaceous connection between Africa and Europe2,26 might have allowed some basal tribosphenic forms to invade northern Africa26. Dryolestoids are present in all bona fide Late Cretaceous localities where mammals are known. This radiation of non-tribosphenic forms was well underway at least by the Cenomanian as evidenced by the highly derived Cronopio, its lineage of sharp-toothed insectivores persisting to the latest Cretaceous, as indicated by Leonardus. Other South American dryolestoids like the mesungulatids developed instead massive bunodont cusps and cingula, adapted to a sophisticated omnivorous/herbivorous diet, and survived into the Palaeocene, forming part of the earliest communities dominated by South American ungulates15,17. The poorly known South American dryolestoid Groebertherium, however, clusters with northern continent dryolestoids and underscores the Pangeic and Jurassic origin of the South American dryolestoid biota, a conclusion also borne out by the extensive ghost lineages implied by the phylogeny presented here (Fig. 5). Tribosphenic molars are held to be a key evolutionary achievement of marsupials, placentals and their closest relatives, that unlocked a wide range of adaptations enabling the colonization of a variety of ecological niches2. Cronopio as well as the South American Late 3 NO V E M B E R 2 0 1 1 | VO L 4 7 9 | N AT U R E | 9 9


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Figure 3 | Cronopio dentiacutus MPCA 454 holotype (upper teeth). a–d, Upper teeth in occlusal (a, d) and labial view (b, c). Scale bar, 3 mm.

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Figure 2 | Cronopio dentiacutus MPCA 454 type skull and MPCA 453 skull and right lower jaw. a, MPCA 454 skull in dorsal (left) right lateral (top right) and left lateral views (bottom right). b, Cronopio dentiacutus MPCA 453 left lateral view of the skull (top left), detail of the petrosal and basicranium (bottom left) and occlusal, labial and lingual views of the right lower jaw (right). Ap, angular process; Cp, coronoid process; Fc, fenestra cochleae; Fv, fenestra vestibuli; Frs, foramen for the ramus superior of the stapedial artery; Mp, masseteric process; VII, facial foramen, for hyomandibular branch of cranial nerve VII. All scale bars are 5 mm, except for bottom-left panel of b, which is 2 mm.

Cretaceous dryolestoids show that we have underestimated both the biological diversity and morphological disparity of the pre-tribosphenic mammals, which present highly derived mammalian morphotypes previously unknown. The equally specialized Cretaceous and/or Palaeocene ferugliotheriid and gondwanatherian27,28 mammals indicate that all Late Cretaceous mammalian groups of South America are endemic to some degree, but how representative dryolestoids and gondwanatheres are of the late Mesozoic faunas of the non-South-American portions of Gondwana is yet unclear. Isolated dental elements from the Late Cretaceous of Africa29 and North America30 lack Cronopio’s autapomorphies, but resemble dryolestoids from the terminal Late Cretaceous of Argentina. At present, the evaluation of those highly fragmentary materials is problematic. Cronopio is an integral part of the evolutionary history leading to the South American mammalian communities of the Late Cretaceous; however, it shares no close ties with prototribosphenidan, australosphenidan or triconodont mammals from the older Middle Jurassic and Early Cretaceous localities of South America. This faunal difference points to a minimum of one major faunal change in South America between the Middle Jurassic and the early Late Cretaceous. Cronopio and other mammals yet to be described from La Buitrera locality are, because of their good preservation and relative completeness, our best hope to address the origin and early evolution of the Mesozoic mammalian faunas of South America. 1 0 0 | N AT U R E | VO L 4 7 9 | 3 NO V E M B E R 2 0 1 1

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Figure 4 | Reconstruction of the skull and jaws of Cronopio dentiacutus based on MPCA 453 and 454. The only areas not preserved in the specimens described here are the lower canines and lower jaw incisors, the septomaxilla, the sagittal crest and part of the cranial vault in the skull. Scale bar, 5 mm. Estimated skull length of MPCA 454 is 27 mm.


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Figure 5 | Simplified phylogenetic tree of the major taxa included in the analysis. The topology reflects a strict consensus tree of 8 equally most parsimonious trees (length 1,114) performed on a matrix including 304 characters and 57 taxa. The dryolestoids (green) show a basal dichotomy with most of the South America forms (dark green) forming a monophyletic group that includes as terminal taxa highly specialized relatively large-sized forms from the Late Cretaceous and Palaeocene. Unlike most other dryolestoids, these derived South American mammals were omnivorous/herbivorous with

complex tooth-on-tooth occlusion and thick enamel, and group together under Mesungulatoidea (see Supplementary Information). Groebertherium from the latest Cretaceous of Argentina appears as a derived member of a northern group of dryolestoids, indicating a probable Jurassic origin from groups of Pangeic distribution for at least some Late Cretaceous South American dryolestoids. Letters at the nodes indicate high-level clades: D, Dryolestoidea; M, Mammalia; Me, Meridiolestida; T, Theria. See Supplementary Information for character list, data matrix and analysis protocol. Myr, million years.

METHODS SUMMARY

5.

Commonly available phylogenetic software (Winclada-Asado, NONA, TNT) was used during the study; see Supplementary Information for search parameters and data sources. Received 15 August; accepted 20 September 2011. 1.

2. 3. 4.

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26. Sigogneau-Russell, D. Further data and reflexions on the tribosphenid mammals (Tribotheria) from the Early Cretaceous of Morocco. Bull. Mus. Natl Hist. Nat. Paris 16, 291–312 (1995). 27. Wilson, G. P., Das Sarma, D. C. & Anantharaman, S. Late Cretaceous sudamericid gondwanatherian mammals from India with paleobiogeographic considerations of Gondwanan mammals. J. Vertebr. Paleontol. 27, 521–531 (2007). 28. Gurovich, Y. & Beck, R. The phylogenetic position of the enigmatic mammalian clade Gondwanatheria. J. Mamm. Evol. 16, 25–49 (2009). 29. Sigogneau-Russell, D. & Ensom, P. C. Thereuodon (Theria, Symmetrodonta) from the Lower Cretaceous of North Africa and Europe, and a brief review of symmetrodonts. Cretac. Res. 19, 445–470 (1998). 30. Fox, R. C. Upper molar structure in the Late Cretaceous symmetrodont Symmetrodontoides Fox, and a classification of the Symmetrodonta (Mammalia). J. Paleontol. 59, 21–26 (1985). Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements We thank M. Salinas, P. A. Gallina and P. J. Makovicky for finding the best specimens; the Avela´s and Pincheira families for logistical support; C. Mun˜oz and R. Barbieri from the MPCA for access to collections under their care; J. A. Gonza´lez and A. Davidson for illustration and technical assistance. Field work permits and loans were facilitated by M. Solorza. C. Corbitt and J. R. Wible read an earlier version of the manuscript. Field work and research was supported by the Antorchas Foundation, American Museum of Natural History and NSF grants DEB 0946430, DEB 1068089 and ATOL 0629959 (to G.W.R.), The Jurassic Foundation (to S.A.) and NASA and Field Museum Womens’ Board (to P. J. Makovicky). This is L.C.G.’s R-46 contribution to the IDEAN. Author Contributions G.W.R. wrote the manuscript with contributions from all authors, edited the figures, scored the matrix and performed the phylogenetic analysis; S.A. edited the manuscript and figures; L.C.G. edited the manuscript, figures, matrix and performed the phylogenetic analysis. Author Information Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of this article at www.nature.com/nature. Correspondence and requests for materials should be addressed to G.W.R. (grougier@louisville.edu).


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