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Digital Reconstruction of the Inner Ear of Leptictidium Auderiense

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Digital Reconstruction of the Inner Ear of Leptictidium Auderiense View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Published in "Paläontologische Zeitschrift 90(1): 153–171, 2016" which should be cited to refer to this work. Digital reconstruction of the inner ear of Leptictidium auderiense (Leptictida, Mammalia) and North American leptictids reveals new insight into leptictidan locomotor agility Irina Ruf1,2 • Virginie Volpato1,3 • Kenneth D. Rose4 • Guillaume Billet2,5 • Christian de Muizon5 • Thomas Lehmann1 Abstract Leptictida are basal Paleocene to Oligocene semicircular canals than the leptictids under study. Our eutherians from Europe and North America comprising estimations reveal that Leptictidium was a very agile ani- species with highly specialized postcranial features mal with agility score values (4.6 and 5.5, respectively) including elongated hind limbs. Among them, the Euro- comparable to Macroscelidea and extant bipedal saltatory pean Leptictidium was probably a bipedal runner or jum- placentals. Leptictis and Palaeictops have lower agility per. Because the semicircular canals of the inner ear are scores (3.4 to 4.1), which correspond to the more gener- involved in detecting angular acceleration of the head, their alized types of locomotion (e.g., terrestrial, cursorial) of morphometry can be used as a proxy to elucidate the agility most extant mammals. In contrast, the angular velocity in fossil mammals. Here we provide the first insight into magnitude predicted from semicircular canal angles sup- inner ear anatomy and morphometry of Leptictida based on ports a conflicting pattern of agility among leptictidans, but high-resolution computed tomography of a new specimen the significance of these differences might be challenged of Leptictidium auderiense from the middle Eocene Messel when more is known about intraspecific variation and the Pit (Germany) and specimens of the North American pattern of semicircular canal angles in non-primate Leptictis and Palaeictops. The general morphology of the mammals. bony labyrinth reveals several plesiomorphic mammalian features, such as a secondary crus commune. Leptictidium Keywords Leptictida Á Leptictidium Á Inner ear Á Bony is derived from the leptictidan groundplan in lacking the labyrinth Á Semicircular canals Á Locomotion secondary bony lamina and having proportionally larger Kurzfassung Leptictida sind basale Eutheria aus dem Pala¨oza¨n bis Oligoza¨n von Europa und Nordamerika, die & Irina Ruf Arten mit hochspezialisiertem Postcranialskelett umfassen; [email protected] so haben manche Arten deutlich verla¨ngerte Hinterbeine. 1 Abteilung Pala¨oanthropologie und Messelforschung, Hierzu geho¨rt die europa¨ische Form Leptictidium, die Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, mo¨glicherweise ein bipeder La¨ufer oder Hu¨pfer war. Da Senckenberganlage 25, 60325 Frankfurt am Main, Germany die Bogenga¨nge des Innenohres die Winkelbeschleunigung 2 Steinmann-Institut fu¨r Geologie, Mineralogie und des Kopfes detektieren, kann deren Morphometrie genutzt Pala¨ontologie, Rheinische Friedrich-Wilhelms-Universita¨t werden, um die Agilita¨t fossiler Sa¨uger zu rekonstruieren. Bonn, Nussallee 8, 53115 Bonn, Germany Erstmals werden hier die Innenohranatomie und – mor- 3 Department of Geosciences, University of Fribourg, Chemin phometrie der Leptictida vorgestellt, die auf hoch- du Muse´e 6, 1700 Fribourg, Switzerland auflo¨senden Computertomografiescans eines neuen 4 Center for Functional Anatomy and Evolution, Johns Exemplares von Leptictidium auderiense aus dem mittleren Hopkins University School of Medicine, 1830 E. Monument Street, Baltimore, MD 21205, USA Eoza¨n der Grube Messel (Deutschland) sowie weiteren Exemplaren der nordamerikanischen Formen Leptictis und 5 Muse´um national d’Histoire naturelle, CR2P - UMR 7207 CNRS, MNHN, Univ Paris 06, Sorbonne Universite´s, 57 rue Palaeictops basieren. Generell zeigt die Morphologie des Cuvier, CP 38, 75005 Paris, France Innenohres, dass die untersuchten Arten zahlreiche plesiomorphe Sa¨ugermerkmale zeigen, wie z. B. ein best represented by the genera Palaeictops and especially sekunda¨res Crus commune. Leptictidium ist vom Grund- Leptictis (Novacek 1977). Palaeictops, a rat-sized animal, plan der Leptictida abgeleitet, da es keine Lamina spiralis is known from the early to the middle Eocene (Rose 1999; ossea secundaria besitzt und proportional gro¨ßere Bogen- Gunnell et al. 2008). With a great number of skulls iden- ga¨nge als die anderen untersuchten Leptictida aufweist. Es tified from Eocene–Oligocene sites, some well-preserved zeigt sich, dass Leptictidium ein recht agiles Tier mit skeletons and even some brain endocasts, Leptictis is cer- Agilita¨tswerten von 4.6 bzw. 5.5 war, die mit denen der tainly the best known leptictidan (Moodie 1922; Butler Macroscelidea und rezenten biped hu¨pfenden Placentalia 1956; Novacek 1977, 1982, 1986; Rose 2006b). vergleichbar sind. Leptictis und Palaeictops haben gerin- The fossil record of the order Leptictida also extends gere Agilita¨tswerte (3.4 bis 4.1), wie bei den meisten into Europe, albeit no attested members of the family rezenten Sa¨ugern, die einen eher generalisierten Lokomo- Leptictidae seem to have been present there (Hooker 2013). tionstyp (z. B. terrestrisch, cursorial) aufweisen. Im The European side of the order is actually represented from Gegensatz dazu zeigt die Berechnung der Winkelbe- the Paleocene to the Eocene by the family Pseudorhynco- schleunigungs-Magnitude, die von den Winkeln zwischen cyonidae (Russell 1964; Sige´ 1974, 1975; Storch and Lister den Bogenga¨ngen abgeleitet wird, ein gegenteiliges Agi- 1985; Mathis 1989; McKenna and Bell 1997; Hooker lita¨tsmuster innerhalb der Leptictida, wobei diese Unter- 2013). Besides the poorly known name-bearing genus schiede weiterer U¨ berpru¨fungen bedu¨rfen, sobald mehr Pseudorhyncocyon (Phosphorites du Quercy, Late Eocene, u¨ber die intraspezifische Variabilita¨t der Bogengangwinkel France), the Paleocene Diaphyodectes and Phakodon,as in Nicht-Primaten bekannt ist. well as the Eocene Fordonia, this family is best charac- terised by the well-documented genus Leptictidium (see Schlu¨sselwo¨rter Leptictida Á Leptictidium Á Innenohr Á Hooker 2013). First described by Tobien (1962) from the kno¨chernes Labyrinth Á Bogenga¨nge Á Lokomotion Messel Pit (Middle Eocene, Germany), Leptictidium is known by several complete skeletons belonging to three Abbreviations species discovered at this site (Koenigswald and Storch AMNH Division of Paleontology, American Museum 1987). Additional but more fragmentary remains of other of Natural History, New York, USA Leptictidium species have been found at Abbey Wood, F-AM Frick Collection, Division of Paleontology, Croydon and Ferry Cliff (Early Eocene, UK) (Hooker American Museum of Natural History, New 2013), Geiseltal (Middle Eocene, Germany) (Storch and York, USA Lister 1985; Hooker 2013), and Phosphorites du Quercy SMF Senckenberg Forschungsinstitut und (Late Eocene, France) (Mathis 1989; Hooker 2013). Naturmuseum Frankfurt, Germany As is well known, the Messel Pit fossils are often very SMF-ME Senckenberg Forschungsinstitut und well preserved and almost complete skeletons, which can Naturmuseum Frankfurt, Germany, Messel sometimes show the imprint of fur and have preserved Collection stomach contents (Koenigswald and Wuttke 1987; Schaal SZ Zoologische Schausammlung, Tu¨bingen, and Ziegler 1992; Koenigswald et al. 1998; Habersetzer Germany and Schaal 2004). In the case of Leptictidium, the stomach USNM Department of Paleobiology, National contents revealed that these animals were omnivores, Museum of Natural History, Smithsonian feeding on insects, lizards, small mammals, and perhaps Institution,Washington DC, USA even some leaves (Maier et al. 1986). Their elongated snout bears features interpreted as linked to the presence of a proboscis (Storch and Lister 1985). Although Leptictid- Introduction ium is one of the most common medium-sized mammals found in the middle Eocene deposits of Messel, details of Terrestrial Paleogene faunas contain various insectivore- its anatomy and ecology are still poorly known and are the like eutherian mammals. Among them, the order Leptic- subject of debates. tida, a group of small to medium-sized animals with For over a century, the relationships of Leptictida have elongate snouts, archaic dentition, and elongated hind been debated. They have been described as stem Placen- limbs, is an intriguing taxon, whose relationships are still talia or alternatively are allied to certain crown Placentalia debated. Representatives of the order Leptictida have been such as Afrotheria, Lipotyphla, Primates, Tupaiidae, and found in North America, Europe, and perhaps Asia (see even Lagomorpha (e.g., Leidy 1868; Matthew 1909; Gre- Kellner and McKenna 1996). The core of the order, how- gory 1910; Simpson 1945; McKenna 1966, 1975; Szalay ever, consists of the Leptictidae, a family known from the 1966, 1977; Butler 1972, 1988; Novacek 1986; MacPhee Paleocene to the Oligocene of North America, which is and Novacek 1993; Asher 1999; Asher et al. 2002, 2003; Rose 2006a; Wible et al. 2007, 2009). Recently, a com- the best extant analogues for leptictidan locomotion are, prehensive study based on morphological data from fossil besides bipedal saltators like Aepyprymnus, Dipodomys and extant mammals combined with molecular sequences and Pedetes, the possibly closely related Macroscelidea (in suggests a sister-group relationship of Leptictida and particular Rhynchocyon),
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