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LETTER doi:10.1038/nature10591

Highly specialized mammalian skulls from the LateCretaceous of South America Guillermo W. Rougier1, Sebastian Apesteguıa2,3 & Leandro C. Gaetano3,4

Dryolestoids are an extinct mammalian group belonging to thelineage leading to modern marsupials and placentals1,2. Dryolestoidsare known by teeth and jaws from the Jurassic period of NorthAmerica and Europe2,3, but they thrived in South America up to theend of the Mesozoic era and survived to the beginnings of theCenozoic2,4–7. Isolated teeth and jaws from the latest Cretaceous of South America provide mounting evidence that, at least in westernGondwana, dryolestoids developed into strongly endemic groups by the Late Cretaceous4–9. However, the lack of pre-Late Cretaceousdryolestoid remains madestudy of theiroriginand earlydiversifica-

tion intractable. Here we describe the first mammalian remainsfrom the early Late Cretaceous of South America, including twopartial skulls and jaws of a derived dryolestoid showing dentaland 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 specializedmasticatory musculature. On one hand, the new mammal sharesderived features of dryolestoids1–3 with forms from the Jurassic of Laurasia, whereas on the other hand, it is very specialized andhighlights the endemic, diverse dryolestoid fauna from theCretaceous of South America. Our specimens include only thesecond 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 non-tribosphenic mammals.

Class Mammalia Linnaeus, 1758Clade Cladotheria McKenna, 1975

Superorder Dryolestoidea Butler, 1939Order Meridiolestida nov.

Cronopio dentiacutus gen. et sp. nov.

Etymology. Cronopio after the fictional, bizarre creatures central tomany stories by Julio Cortazar; dentiacutus, from Latin, meaning sharp, acute teeth.Holotype. MPCA454 (Museo Provincial Carlos Ameghino, Cipolletti,Rıo Negro Province, Argentina), an incomplete skull preserving a full

upper dentition, but missing the braincase, part of the rostral roof andthe lower jaws (Figs 1–4).Localityand horizon. CandelerosFormation(Cenomanian),NeuquenGroup10. The specimens come from the La Buitrera locality, Rıo NegroProvince, Argentina, that has yielded abundant skeletons of small

vertebrates11,12 and dinosaurs13,14. See Supplementary Informationfor further data on age, systematics and morphology .Diagnosis and description. Medium-sized dryolestoid, with anextremely elongated rostrum, extended edentulous portion of the pre-maxilla, and orbits placed dorsally because of a tall zygoma with adeeply 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 compressedmolariforms. Upper and lower premolars are supported by two rootswhereasthe molars rest on a single labiolingually broad root. Thelower

jaw (Figs 1–2 and 4) possesses a masseteric process that juts outlaterally forminga broad platform whereas the angular process is smalland medially inflected. Cronopio differs from other South Americandryolestoids like Leonardus cuspidatus4,8 in having a contact betweenthestyloconeand paracrista, with a stylocone notas large, thepresenceof a distinct small parastylar hook andat least one less molar.Cronopioand other South American dryolestoids4,7,15 share the presence of a

posterior premolar (P3 in Cronopio) with a small anterior cusp sup-ported 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 otherSouth American dryolestoids share with all other dryolestoids a muchtaller labial crown height than lingual in the lower molars (the reversein the uppers), a small talonid, a relatively transverse metacristid, andmesiodistally compressed trigonids1–3 (Figs 1–4).

Cronopio’s canine is extremely long and moderately compressedbuccolingually. The dryolestoid Drescheratherium from the Jurassicof Portugal16 also shows very long canines but not to the extent of Cronopio. A distinctive feature of Cronopio and several SouthAmerican dryolestoids is thepresenceof complex penultimate and fully molarized ultimate premolars7–15. The penultimate premolar coincides

with a sharp constriction of the rostrum, leaving a much lower anterioraccessory cusp isolated from the moderately basined posterior half of the tooth. This unusual morphology, although with a better developedbasin, served as the basis for the recognition of several Late Cretaceoustaxa such as Barberenia and Quirogatherium5,6, which in light of thenew evidence probably represent just the penultimate premolar posi-tion of other taxa4,5,17 described based on molars. Similarly shapedteethareknownforthe mesungulatidsColoniatherium8, Mesungulatum4–6,17

and Peligrotherium7,15, although only for Peligrotherium is the positionof the tooth P2 known unambiguously, indicating that this is a con-spicuous feature of many South American dryolestoids. Previousstudies5,17,18 have recognized two species of triconodont mammals inthe Late Cretaceous Los Alamitos Formation; the morphology of theteeth referred to these species is similar to that of the anterior upper

and lower premolars of Cronopio and Peligrotherium. We suggest thatthese putative triconodonts represent anterior premolar positions of dryolestoids (see Supplementary Information). Upper and lowermolars of Cronopio (Fig. 4) are highly compressed mesiodistally andaresingle-rooted. Theupper crownsare dominatedby a paracone anda stylocone connected to the paracrista. Both, premolars and molarsare arranged forming a gentle arch that curves posteriorly along themaxillary border. The simultaneous presence of single-rooted molarsand double-rooted premolars is a unique feature distinguishing Cronopio from any other Mesozoic mammal.

Cronopio’s skull shows a combination of primitive mammalianfeatures and highly specialized traits. Cronopio shares with basal

1Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, Kentucky 40202, USA. 2CEBBAD - Fundacion de Historia Natural ‘Felix de Azara’, Universidad Maimonides,

Hidalgo 775, Buenos Aires (1405), Argentina. 3CONICET, Consejo Nacional de Investigaciones Cientıficas y Tecnicas. Av. Rivadavia 1917, C1033AAJ, Buenos Aires, Argentina. 4Departamento de Cs.

Geologicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellon II, C1428EHA, Buenos Aires, Argentina.

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mammaliaforms features such as the presence of a septomaxilla, ananterior lamina of the petrosal, a lateral flange, and all the elements of cranial circulation thought to be primitive for therians, including afully developed stapedial system19. The snout of Cronopio is unusually long and narrow with a relatively large orbit, a small temporal areaand a robust zygoma deeply excavated by a masseteric fossa. Thecraniodental morphology, in particular the low coronoid processand the hyperdeveloped masseteric fossa and process, indicates thatCronopio emphasized rotation of the jaws during mastication at theexpense of a powerful bite20. With the exception of a fully definitivemammalian middle ear21, Cronopio shows that the major changes inskull morphology characterizing the hypotheticalcommon ancestorof marsupials and placentals22 were not yet established in dryolestoidsand that theyretained not onlya primitivenon-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 SouthAmerican dryolestoids (see Supplementary Information). Leonardusand other Cretaceous South American dryolestoids are successivesister groups reflecting the establishment of a Cretaceous endemicbiota4,5. Although in theCretaceous of Laurasia marsupialand placental(therians) relatives were major components of the fauna, they are yetto 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 mammalswouldalso be originally absentfrom those continents duringthe Jurassic andearliest Cretaceous, despite Africa–Europe contacts during theCretaceous2,26. However, an Early Cretaceous connection betweenAfrica and Europe2,26 might have allowed some basal tribosphenicforms to invade northern Africa26. Dryolestoidsare present in allbonafide Late Cretaceous localities where mammals are known. This radi-ation of non-tribosphenic forms was well underway at least by theCenomanian as evidenced by the highly derived Cronopio, its lineageof sharp-toothed insectivores persisting to the latest Cretaceous, asindicated by Leonardus. Other South American dryolestoids like themesungulatids developed instead massive bunodont cusps andcingula, adapted to a sophisticated omnivorous/herbivorous diet,and survived into the Palaeocene, forming part of the earliest com-munities dominated by South American ungulates15,17. The poorly known South American dryolestoid Groebertherium, however,clusters with northern continent dryolestoids and underscores thePangeic 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 achievementof marsupials, placentals and their closest relatives, that unlocked awide range of adaptations enabling the colonization of a variety of

ecological niches2. Cronopio as well as the South American Late

a b

c

d

e

Figure 1 | Cronopio dentiacutus MPCA 454type skull and MPCA 453rightlowerjaw. a –c, MPCA 454 skull in ventral (a ) anddorsal views (b); labial view of the left upper dentition (c). d, e, Cronopio dentiacutus MPCA 453 right lower jawin labial and lingual views (d) anddetail of theleft petrosal andbasicranium (e).

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Cretaceous dryolestoids show that we have underestimated both thebiological diversity and morphological disparity of the pre-tribosphe-nic mammals, which present highly derived mammalian morphotypespreviously unknown.

The equally specialized Cretaceous and/or Palaeocene ferugliotheriidand gondwanatherian27,28 mammals indicate that all Late Cretaceousmammalian groups of South America are endemic to some degree,but how representative dryolestoids and gondwanatheres are of the lateMesozoic faunas of the non-South-American portions of Gondwana isyetunclear.Isolateddental elementsfromthe LateCretaceousof Africa29

and North America30 lack Cronopio’s autapomorphies, but resembledryolestoidsfromthe terminal LateCretaceous of Argentina.At present,the evaluation of those highly fragmentary materials is problematic.

Cronopio is an integralpartof theevolutionary historyleadingto theSouth American mammalian communities of the Late Cretaceous;however, it shares no close ties with prototribosphenidan, australo-sphenidan or triconodont mammals from the older Middle Jurassicand Early Cretaceous localities of South America. This faunal differ-ence points to a minimum of one major faunal change in SouthAmerica between the Middle Jurassic and the early Late Cretaceous.Cronopio and other mammals yet to be described from La Buitreralocality are, because of their good preservation and relative complete-ness, our best hope to address the origin and early evolution of the

Mesozoic mammalian faunas of South America.

a c db

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

a

c

b

Figure 4 | Reconstruction of the skull and jaws of Cronopio dentiacutus based on MPCA 453 and 454. The only areas not preserved in the specimensdescribed 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.

a

b

Fv

Mp

Mp

Ap

Cp

Frs

Fc

VII

Figure 2 | Cronopio dentiacutus MPCA 454type skull and MPCA 453 skullandright lower jaw. a , MPCA 454skull in dorsal(left) right lateral (top right)and left lateral views (bottom right). b, Cronopio dentiacutus MPCA 453 leftlateral view of theskull (top left),detail of thepetrosal andbasicranium (bottomleft) 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 cranialnerve VII. All scale bars are 5 mm, except for bottom-left panel of b, which is2mm.

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METHODS SUMMARY

Commonly available phylogenetic software (Winclada-Asado, NONA, TNT) wasused during the study; see Supplementary Information for search parameters anddata sources.

Received 15 August; accepted 20 September 2011.

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Mesungulatum

Coloniatherium

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Reigitherium

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Cronopio

Foxraptor

Paurodon

Drescheratherium

Henkelotherium

Dryolestes

Laolestes

Amblotherium

Comotherium

Groebertherium

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Australosphenidans

Morganucodontids

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Figure 5 | Simplified phylogenetic tree of the major taxa included in theanalysis. The topology reflects a strict consensus tree of 8 equally mostparsimonious trees (length 1,114) performed on a matrix including 304characters and 57 taxa. The dryolestoids (green) show a basal dichotomy withmost of the South America forms (dark green) forming a monophyletic groupthat includes as terminal taxa highly specialized relatively large-sized formsfromthe Late Cretaceous and Palaeocene.Unlikemost otherdryolestoids, thesederived South American mammals were omnivorous/herbivorous with

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

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Supplementary Information is linked to the online version of the paper atwww.nature.com/nature.

Acknowledgements We thank M. Salinas, P. A. Gallina and P. J. Makovicky for findingthe bestspecimens;the Avelas and Pincheira families for logistical support; C. Mun ozandR. Barbieri fromthe MPCAfor access to collectionsundertheircare; J. A. Gonzalezand A. Davidsonfor illustrationand technical assistance. Field workpermitsand loanswere facilitated by M. Solorza. C. Corbitt and J. R. Wible read an earlier version of themanuscript. Field work and research was supported by the Antorchas Foundation,American Museum of Natural History and NSF grants DEB 0946430, DEB 1068089andATOL0629959 (toG.W.R.), The Jurassic Foundation (toS.A.) andNASAand FieldMuseum Womens’ Board (to P.J. Makovicky). This is L.C.G.’s R-46contribution to theIDEAN.

Author Contributions G.W.R. wrote themanuscriptwithcontributionsfrom allauthors,

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 andperformed the phylogenetic analysis.

Author Information Reprints and permissions information is available atwww.nature.com/reprints. The authors declare no competing financial interests.Readers are welcome to comment on the online version of this article atwww.nature.com/nature. Correspondence and requests for materials should beaddressed to G.W.R. ([email protected]) .

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