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Skeleton of a Cretaceous Mammal from Madagascar Reflects Long-Term Insularity

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Article Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity https://doi.org/10.1038/s41586-020-2234-8 David W. Krause1,2 ✉, Simone Hoffmann3, Yaoming Hu2,15, John R. Wible4, Guillermo W. Rougier5, E. Christopher Kirk6,7, Joseph R. Groenke2,8, Raymond R. Rogers9, Received: 5 November 2019 James B. Rossie10, Julia A. Schultz11, Alistair R. Evans12,13, Wighart von Koenigswald11 & Accepted: 26 February 2020 Lydia J. Rahantarisoa14 Published online: xx xx xxxx Check for updates 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 teeth1–5. 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. Island environments promote evolutionary trajectories among mam- even non-osseous tissues (such as costal cartilage) are preserved in articular mals and other vertebrates that contrast with those on continents, and relationships. A. hui has an estimated body mass of about 3.1 kg (Extended which result in demonstrable anatomical, physiological and behav- Data Fig. 2, Supplementary Information, Supplementary Table 1). As such, ioural differences6–10. These differences have previously been ascribed it is the third-largest known mammal represented by anything more than to markedly distinct selection regimes that involve factors such as isolated jaws and teeth from the Mesozoic era of Gondwana, despite the limited resources, reduced interspecific competition and a paucity of fact that it is represented by an immature individual. predators and parasites6,7,9–13. Although there are numerous examples Gondwanatheria, a clade restricted to Late Cretaceous and Palaeo- of insular effects on mammals of the Cenozoic era6–12,14–17, the effects of gene horizons of Gondwana, is particularly poorly represented in the long-term isolation on islands are virtually unknown among Mesozoic fossil record4,5. Prior to the discovery reported here, the cranium of Vin- mammaliaforms, and Mesozoic biotas more generally. Here we describe tana—also from the latest Cretaceous period of Madagascar—was the only and analyse a complete, well-preserved skeleton of a gondwanathe- gondwanatherian represented by more than isolated dental or gnathic rian mammal (Fig. 1, Extended Data Fig. 1) from the latest Cretaceous remains3,4. The new fossil greatly expands our knowledge of gondwanathe- period of Madagascar, which was then—and still remains—an island. rians and of Mesozoic mammaliaforms from Gondwana in general, the This skeleton reveals an array of unusual and even unique adaptations fossil record of which is extremely limited relative to that of Laurasia1,2. that we hypothesize are due to evolution in an insular environment. The new specimen—designated University of Antananarivo (UA) 9030—is Mammalia, Linnaeus 1758 the holotype of a new genus and species of gondwanatherian, Adalatherium Allotheria, Marsh 1880 hui, which we assign to the new family Adalatheriidae. UA 9030 is so well pre- Gondwanatheria, Mones 1987 served that the distalmost caudal vertebrae, tiny phalangeal sesamoids and 1Department of Earth Sciences, Denver Museum of Nature and Science, Denver, CO, USA. 2Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA. 3Department of Anatomy, College of Osteopathic Medicine, New York Institute of Technology, Old Westbury, NY, USA. 4Section of Mammals, Carnegie Museum of Natural History, Pittsburgh, PA, USA. 5Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, USA. 6Department of Anthropology, University of Texas at Austin, Austin, TX, USA. 7Jackson School Museum of Earth History, University of Texas at Austin, Austin, TX, USA. 8Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, OH, USA. 9Geology Department, Macalester College, St Paul, MN, USA. 10Department of Anthropology, Stony Brook University, Stony Brook, NY, USA. 11Institut für Geowissenschaften, Universität Bonn, Bonn, Germany. 12School of Biological Sciences, Monash University, Clayton, Victoria, Australia. 13Geosciences, Museums Victoria, Melbourne, Victoria, Australia. 14Département de Sciences de la Terre et de l’Environnement, Université d’Antananarivo, Antananarivo, Madagascar. 15Deceased: Yaoming Hu. ✉e-mail: [email protected] Nature | www.nature.com | 1 Article a Lumbar vertebrae Hindlimb (r) Ribs Caudal vertebrae Scapula (l) Skull Pelvis Forelimb (r) Forelimb (l) Hindlimb (l) b Fig. 1 | Skull and postcranial skeleton of A. hui holotype (UA 9030). a, ‘Top’ view, as preserved. Scale bar, 5 cm. b, Reconstruction in left lateral view. Left and right sides indicated as (l) and (r), respectively. Adalatheriidae Krause, Hoffmann, Wible, and Rougier, 2020, fam. nov. Adalatherium hui Krause, Hoffmann, Wible, and Rougier, 2020, gen. Diagnosis. A. hui differs from all other known Mesozoic mammalia- et sp. nov. forms in possessing quadrangular upper postcanine tooth crowns with four major cusps and three connecting perimetric ridges mesially, Etymology. Adàla (Malagasy), ‘crazy’; therium (Latinized form of the lingually and distally that border—on three sides—a central valley that Greek θηριον), ‘beast’; the species name hui is in reference to the late opens buccally; and lower postcanine tooth crowns with four major Yaoming Hu for his contributions to our knowledge of early mammals. cusps arranged in a diamond pattern and connected by four perimetric crests, and a prominent mesiobuccal basin on the two distalmost lower postcanines. The full diagnosis is provided in the Supplementary Holotype. UA 9030, skull and postcranial skeleton. Information. Type locality and horizon. MAD99-15, Berivotra study area (north- western Madagascar). Upper Cretaceous series (Maastrichtian stage, Cranium 72.1–66 million years (Myr) ago), Anembalemba Member, Maevarano The cranium of Adalatherium reveals a mosaic of plesiomorphic and de - Formation, Mahajanga Basin18. Additional information on the geological rived features (Fig. 2a–d, Extended Data Fig. 3, Supplementary Videos 1–3). context is provided in the Supplementary Information. The presence of a very large internasal vacuity, five infraorbital foramina, 2 | Nature | www.nature.com a b Squamosal Jugal Canine Nasal foramina Distal Petrosal Internasal incisor vacuity Mesial Occipital Alisphenoid PC1 incisor PC5 PC4 PC3 PC2 ? Mesial ? incisors Maxilla Premaxilla Nasal Occipital Frontal Septomaxilla Incisive foramen Temporal Maxilla Glenoid Temporal Petrosal Squa- Lacrimal fenestra fossa fenestra Orbit mosal Orbit Premaxilla Foramen for ethmoidal nerve (V1) Jugal Internasal vacuity c d Nasal Nasal foramina Septomaxillary canal Frontal Lacrimal foramen Foramen for ? Lacrimal ethmoidal nerve (V1) Frontal Foramen for ethmoidal nerve (V1) Lacrimal Sphenorbital Nasal Nasal ssure Septomaxilla Maxilla cavity Alisphenoid Orbit Infraorbital foramina Jugal Squamosal Jugal Premaxilla Canine PC4 PC3 PC2 PC1 Petrosal PC5 Septomaxilla Distal incisor Infraorbital Canine Mesial incisor Occipital Premaxilla Mesial incisor foramina Distal incisor e Coronoid IncisorIncisor Condyle Condyle process fgpc3 pc4 pc3 pc2 pc4 pc3pc2 pc2 pc1 Pterygoid pc1 Mental fossa Masseteric foramen pc1c1 fossa Incisor Incisor Condyle Coronoid process Symphysis Mandibular foramen Pterygoid shelf hijk PC5 PC4 PC3 PC2 PC1 PC5 PC4 PC3 PC2 PC1 l pc4 pc3 pc2 pc1 mnpc4pc3 pc2 pc1 Mesiobuccal basin Fig. 2 | Cranium, lower jaw and dentition of A. hui holotype (UA 9030). in occlusal view (k). l–n, μCT digital renderings of right lower dentition, a–d, Reconstructed cranium in dorsal (a), ventral (b), right lateral (c) and showing the postcanine teeth (l) and incisor (m) in buccal views, and the anterior (d) views. e–g, Reconstructed right lower jaw in lateral (e), dorsal postcanine teeth in occlusal view (n). Scale bars, 2 cm (a–g; scale bar above e ( = occlusal) (f) and medial (g) views. h–k, Micro-computed tomography (μCT) and f applies to a–g), 5 mm (h–n). PC, upper postcanine tooth; pc, lower digital renderings of right upper dentition, showing the postcanine teeth (h), postcanine tooth. distal incisor (i) and mesial incisor (j) in buccal views, and the postcanine teeth a large foramen in the lacrimal that is not related to the nasolacrimal septomaxilla with prominent posterodorsal and intranarial
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  • Osteohistology of Late Triassic Prozostrodontian Cynodonts from Brazil

    Osteohistology of Late Triassic Prozostrodontian Cynodonts from Brazil

    Osteohistology of Late Triassic prozostrodontian cynodonts from Brazil Jennifer Botha-Brink1,2, Marina Bento Soares3 and Agustín G. Martinelli3 1 Department of Karoo Palaeontology, National Museum, Bloemfontein, South Africa 2 Department of Zoology and Entomology, University of the Free State, Bloemfontein, South Africa 3 Departamento de Paleontologia e Estratigrafia, Instituto de Geociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil ABSTRACT The Prozostrodontia includes a group of Late Triassic-Early Cretaceous eucynodonts plus the clade Mammaliaformes, in which Mammalia is nested. Analysing their growth patterns is thus important for understanding the evolution of mammalian life histories. Obtaining material for osteohistological analysis is difficult due to the rare and delicate nature of most of the prozostrodontian taxa, much of which comprises mostly of crania or sometimes even only teeth. Here we present a rare opportunity to observe the osteohistology of several postcranial elements of the basal prozostrodontid Prozostrodon brasiliensis, the tritheledontid Irajatherium hernandezi, and the brasilodontids Brasilodon quadrangularis and Brasilitherium riograndensis from the Late Triassic of Brazil (Santa Maria Supersequence). Prozostrodon and Irajatherium reveal similar growth patterns of rapid early growth with annual interruptions later in ontogeny. These interruptions are associated with wide zones of slow growing bone tissue. Brasilodon and Brasilitherium exhibit a mixture of woven-fibered bone tissue and slower growing parallel-fibered and lamellar bone. The slower growing bone tissues are present even during early ontogeny. The relatively slower growth in Brasilodon and Brasilitherium may be related to their small body size compared to Prozostrodon and Irajatherium. These brasilodontids also exhibit osteohistological similarities with the Late Triassic/Early Jurassic mammaliaform Morganucodon and the Late Cretaceous multituberculate mammals Kryptobaatar and Nemegtbaatar.
  • Microvertebrates of the Lourinhã Formation (Late Jurassic, Portugal)

    Microvertebrates of the Lourinhã Formation (Late Jurassic, Portugal)

    Alexandre Renaud Daniel Guillaume Licenciatura em Biologia celular Mestrado em Sistemática, Evolução, e Paleobiodiversidade Microvertebrates of the Lourinhã Formation (Late Jurassic, Portugal) Dissertação para obtenção do Grau de Mestre em Paleontologia Orientador: Miguel Moreno-Azanza, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Co-orientador: Octávio Mateus, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Júri: Presidente: Prof. Doutor Paulo Alexandre Rodrigues Roque Legoinha (FCT-UNL) Arguente: Doutor Hughes-Alexandres Blain (IPHES) Vogal: Doutor Miguel Moreno-Azanza (FCT-UNL) Júri: Dezembro 2018 MICROVERTEBRATES OF THE LOURINHÃ FORMATION (LATE JURASSIC, PORTUGAL) © Alexandre Renaud Daniel Guillaume, FCT/UNL e UNL A Faculdade de Ciências e Tecnologia e a Universidade Nova de Lisboa tem o direito, perpétuo e sem limites geográficos, de arquivar e publicar esta dissertação através de exemplares impressos reproduzidos em papel ou de forma digital, ou por qualquer outro meio conhecido ou que venha a ser inventado, e de a divulgar através de repositórios científicos e de admitir a sua cópia e distribuição com objetivos educacionais ou de investigação, não comerciais, desde que seja dado crédito ao autor e editor. ACKNOWLEDGMENTS First of all, I would like to dedicate this thesis to my late grandfather “Papi Joël”, who wanted to tie me to a tree when I first start my journey to paleontology six years ago, in Paris. And yet, he never failed to support me at any cost, even if he did not always understand what I was doing and why I was doing it. He is always in my mind. Merci papi ! This master thesis has been one-year long project during which one there were highs and lows.