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A Radiation of Arboreal Basal Eutherian Mammals Beginning in the Late Cretaceous of India

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A Radiation of Arboreal Basal Eutherian Mammals Beginning in the Late Cretaceous of India A radiation of arboreal basal eutherian mammals beginning in the Late Cretaceous of India Anjali Goswamia,b,1, Guntupalli V. R. Prasadc, Paul Upchurchb, Doug M. Boyerd, Erik R. Seifferte, Omkar Vermaf, Emmanuel Gheerbrantg, and John J. Flynnh aDepartment of Genetics, Evolution, and Environment, bDepartment of Earth Sciences, University College London, London WC1E 6BT, United Kingdom; cDepartment of Geology, Centre for Advanced Studies, University of Delhi, Delhi 110 007, India; dDepartment of Anthropology and Archaeology, Brooklyn College, City University of New York, Brooklyn, NY 11210; eDepartment of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-8081; fSchool of Sciences, Indira Gandhi National Open University, New Delhi 110 068, India; gUnité Mixte de Recherche 7207 du Centre National de la Recherche Scientifique (CR2P), Département Histoire de la Terre, Muséum National d’Histoire Naturelle, 75005 Paris, France; and hDivision of Paleontology and Richard Gilder Graduate School, American Museum of Natural History, New York, NY 10024 Edited* by Elwyn L. Simons, Duke University, Durham, NC, and approved August 15, 2011 (received for review June 6, 2011) India’s Late Cretaceous fossil mammals include the only undis- cluding placentals and their stem relatives) are known from the puted pre-Tertiary Gondwanan eutherians, such as Deccanolestes. Late Cretaceous of Laurasia (North America, Europe, and Asia) Recent studies have suggested a relationship between Deccano- (9), and although a few have been suggested as possible pla- lestes and African and European Paleocene adapisoriculids, which centals [e.g., Protungulatum (10)], none are unequivocally sup- have been variably identified as stem euarchontans, stem pri- ported as a Cretaceous placental mammal (2). With over 4,969 mates, lipotyphlan insectivores, or afrosoricids. Support for a close small-mammal fossils recovered from Mesozoic deposits world- relationship between Deccanolestes and any of these placental wide (ref. 9: occurence matrix downloaded using the parameters fi mammal clades would be unique in representing a con rmed Me- taxon = Mammalia, interval = Cretaceous; species data down- sozoic record of a placental mammal. However, some paleogeo- loaded using the parameters: taxon = Eutheria, interval = graphic reconstructions place India at its peak isolation from all Cretaceous), the absence of placentals cannot easily be ascribed other continents during the latest Cretaceous, complicating recon- to unsuitable preservation conditions across such a broad spec- structions of the biogeographic history of the placental radiation. EVOLUTION trum of temporal, geographic, and paleoenvironmental settings Recent fieldwork in India has recovered dozens of better-pre- (11). One possible explanation for the contradiction between the served specimens of Cretaceous eutherians, including several observed record and molecular age estimates is that molecular new species. Here, we incorporate these new specimens into an fl extensive phylogenetic analysis that includes every clade with a clocks for placentals may be awed and inaccurately reconstruct previously hypothesized relationship to Deccanolestes. Our results estimated divergence ages. Alternatively, some of the described support a robust relationship between Deccanolestes and Paleo- Cretaceous eutherians may be stem members of particular pla- cene adapisoriculids, but do not support a close affinity between cental lineages, but had not yet evolved the osteological syna- these taxa and any placental clade, demonstrating that Deccano- pomorphies of their crown clades, the presence of which would lestes is not a Cretaceous placental mammal and reinforcing the be necessary for accurate cladistic placement. Finally, Late sizeable gap between molecular and fossil divergence time esti- Cretaceous placentals may exist, but remain unsampled if pla- mates for the placental mammal radiation. Instead, our expanded centals originated where the fossil record is poor, specifically in data push Adapisoriculidae, including Deccanolestes, into a much the Late Cretaceous of Gondwana (11) [South America, Africa, more basal position than in earlier analyses, strengthening hypoth- Antarctica, Madagascar, India, and Australia: fewer than 5% of eses that scansoriality and arboreality were prevalent early in euthe- Cretaceous fossil mammal localities are Gondwanan (9)]. rian evolution. This comprehensive phylogeny indicates that faunal Among Gondwanan landmasses, India has been of particular exchange occurred between India, Africa, and Europe in the Late interest for decades (12), since the discovery of the first un- Cretaceous-Early Paleocene, and suggests a previously unrecognized disputed Cretaceous Gondwanan eutherian, Deccanolestes hislopi ∼30 to 45 Myr “ghost lineage” for these Gondwanan eutherians. (13). The Indian subcontinent’s lengthy northward migration, starting with Gondwanan breakup from the Middle Jurassic (178– placentals | paleobiogeography | phylogenetics | dispersal 161 Mya) to its collision with Asia in the Eocene (14), has fueled discussions about an Indian “Garden of Eden” for placental espite substantial augmentation of the Mesozoic record of mammals (12). To date, five species of eutherians have been Dmammals and improvements in calibration methods for named from India’s Upper Cretaceous (Maastrichtian, 70.6– molecular clock estimators, the age of origin of placental mam- 65.5 Mya) intertrappean beds: D. hislopi (13), Deccanolestes mals remains hotly debated (1, 2). Molecular clock estimates robustus (15), Deccanolestes narmadensis (16), Sahnitherium ran- consistently place the earliest divergences within Placentalia as gapurensis (17), and Kharmerungulatum vanvaleni (18). Sahnithe- falling within the Late Cretaceous (99.6–65.5 Mya) (3), or even rium is known from only a single molar and has been qualitatively – in the Early Cretaceous (145.5 99.6 Mya) (1), but the existence compared with “zhelestids,” but also shares many morphological of placental fossils from pre-Paleocene (older than 65.5 Mya) similarities with Deccanolestes (17) (see Materials and Methods). deposits is highly contentious (2). These ancient molecular di- Kharmerungulatum is also known from a single, heavily worn vergence age estimates and the absence of Cretaceous placentals can be reconciled by proposing that the first 20 to 40 Myr (or 25– ’ 50%) of this group s fossil record is missing entirely. A few re- Author contributions: A.G., G.V.R.P., P.U., and D.M.B. designed research; A.G., G.V.R.P., cent studies using statistical models that incorporate gaps in the D.M.B., E.R.S., O.V., E.G., and J.J.F. performed research; A.G. and P.U. analyzed data; and fossil record to estimate divergence times, either from fossil A.G. wrote the paper. occurrences alone or combined with molecular data, have pro- The authors declare no conflict of interest. duced results more similar to molecular clock dates (81–88 Mya) *This Direct Submission article had a prearranged editor. for the origin of Primates (4, 5), but other quantitative analyses 1To whom correspondence should be addressed. E-mail: [email protected]. based on the fossil record dispute these early divergence esti- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. mates (6–8). At least 70 species of eutherians (the clade in- 1073/pnas.1108723108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1108723108 PNAS Early Edition | 1of6 Downloaded by guest on September 30, 2021 molar, and was described as a possible placental mammal, specifi- cally a “condylarth” (18). D. hislopi is the only Indian Cretaceous eutherian to have been included in a few previous phylogenetic analyses, which have returned mixed results. Analyses based on the first described, heavily worn dental specimens placed Deccanolestes as a stem eutherian, outside of placentals (2), consistent with the “paleo- ryctid-like” dental morphology noted in its original description (13). In contrast, phylogenetic analyses based on tarsal elements, which show arboreal specializations such as an enlarged peroneal tubercle of the calcaneum and confluence of the navicular and sustentacular facets (19) (Fig. S1), have placed Deccanolestes as a stem member of Euarchonta (primates, colugos, and tree shrews), well within Placentalia (20). However, recent qualitative studies have suggested a relationship between Deccanolestes and African and European Paleocene adapisoriculids (16, 21, 22)— which have been variably identified as stem euarchontans (21), stem primates (23), lipotyphlan insectivores (24), or afrosoricids (25)—but this relationship has never been tested with a phylo- genetic analysis. Support for a close relationship between Dec- canolestes and any of these placental mammal clades would be unique in representing a confirmed Mesozoic fossil record of a placental mammal. At present then, Deccanolestes and Khar- merungulatum represent some of the best potential evidence for pre-Tertiary placentals, and thus lie at the heart of resolving the debate over the timing of placental origins. Fig. 1. Relationships of Deccanolestes to other eutherians. Simplified re- Recent discoveries of many more and better-preserved dental, duced strict consensus tree using the Exafroplacentalia crown group con- mandibular (16), and postcranial (22) specimens, the result of straint. Shaded area, Cretaceous period (145.5–65.5 Mya). Positions of years of fieldwork in Central and South India, provide an op- terminal branches indicate the
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