Cochlea anatomy of Numidotherium koholense: auditory acuity in the oldest known proboscidean

Court, N. 1992 04 15: Cochlea anatomy of Numidotherium koholense: auditory acuity in the oldest known proboscidean. Lethaia , Vol. 25, pp. 211–215. Oslo. ISSN 0024–1164.
A natural cast of the spiral cochlea space from the inner ear of the oldest known proboscidean, Numidotherium koholense , is described. The cast was sectioned to reveal internal structures. Cochlea structure in numiodtheres, and by inference auditory acuity, is shown to have been very different from that of living proboscideans. The cochlea of Numidotherium is deemed to reflect tuning to relatively high frequencies and contrasts with the low-frequency specializations seen in the inner ear of living proboscideans. It is suggested that evolution of the elephant otic region might be explained by a shift in developmental timing such that features occurring earlier in ontogeny are characteristic of the adult stage. * Proboscidea, Numidotherium, cochlea, natural cast, auditory acuity .     

L’origine et l’évolution des éléphants

Origin and evolution of proboscideans. Recent palaeontological research has significantly enhanced our knowledge of the evolution of proboscideans, especially the beginning of their evolutionary history. New discoveries in the Early Eocene support, in particular, a lophodont ancestral morphotype for the Proboscidea and the African origin of the order, from which the Asiatic Anthracobunidae are excluded. The primitive Eocene proboscideans remain, however, poorly known. Other important discoveries have been made on the question of the origin of the moeritheres, of the deinotheres and elephantimorphs, and on the differentiation of elephantids. Palaeontology demonstrates in the Proboscidea a remarkably rich history, unsuspected from the extant relictual diversity, and one of the most spectacular morphological evolutions in the Mammalia.     

Evolution of the tooth enamel microstructure in the earliest proboscideans (Mammalia)

Microstructural features of the mammalian tooth enamel are rarely used to construct phylogenies, although macromorphological characters of the dentition figure prominently in phylogenetic analysis. In order to test the phylogenetic significance of the enamel microstructures, we investigate here the earliest proboscideans recently found in the Early Palaeogene of Africa (e.g. Phosphatherium , Daouitherium , Khamsaconus , and Numidotherium ). The results are discussed in the light of the recent advances concerning the intra- and interordinal relationships of the Proboscidea. We also consider other basal paenungulates such as 'anthracobunids', embrithopods, and hyraxes. The analysed microstructures suggest that the enamel ancestral morphotype of paenungulates was primitive for eutherian mammals, consisting in radial enamel. Some basal proboscideans developed decussations of prisms in Hunter-Schreger bands (HSB), as did most of the medium to large-sized mammals. More evolved proboscideans developed very complex enamel, the 3-D enamel, which represents an apomorphy for the group. The three-layered Schmelzmuster, typical of the elephantoids (3-D enamel, HSB, and radial enamel), is acquired during the late Eocene with the enigmatic ' Numidotherium ' savagei . This species is here considered as an advanced proboscidean along with Moeritherium -Deinotheriidae-Elephantiformes. The peculiar enamel of elephantoids arose step by step. Although homoplasy and mosaic evolution occur, the enamel microstructures represent an important source of new dental characters for phylogenetic reconstructions. As macromorphological characters testified, the diversity of the enamel microstructures observed in the various basal proboscideans illustrates an unexpected early diversity of the order in Africa.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 149 , 611–628.     

Unique differentiation of radial enamel in Arsinoitherium (Embrithopoda,Tethytheria)

The enamel microstructure in molars of Arsinoitherium is reinvestigated and a new modification of radial enamel (RE), ‘arsinoitheriid radial enamel (ARE)’, is defined. It is characterised by alternating stripes with different organisation of the interprismatic matrix but no prism decussation. Recognition of this new subtype leads to a reinterpretation of structure previously identified as modified radial enamel and of Hunter–Schreger bands in Arsinoitherium. The newly differentiated ARE of Arsinoitherium is more derived in relation to corresponding microstructures of Palaeoamasia and Crivadiatherium. A careful reinvestigation of RE in other Paenungulata will be required to provide additional data bearing on phylogenetic reconstruction. The enamel of Phenacolophus argues against inclusion of this genus in the Embrithopoda.     

Anatomy and phylogenetic value of the mandibular and coronoid canals and their associated foramina in proboscideans (Mammalia)

Characters associated with the mandibular canal are differently distributed amongst proboscidean lineages and provide useful information on the systematics and relationships of proboscideans. The aim of this paper is to describe the pattern of the mandibular canal and its associated foramina in proboscideans in order to fully appreciate the extent of interspecific variation of these structures within the group and to discuss its systematic and phylogenetic value. Outgroup comparison indicates that the condition presented by the basal proboscidean Phosphatherium is morphotypic for proboscideans. Primitive proboscidean characters are: the low position of the mandibular foramen, and its crescent‐shaped outline, the occurrence of a coronoid foramen (canal), the occurrence of two lateral mental foramina, the posterior one at the level of (or slightly behind) the posterior margin of the symphysis, the anterior one in a more distal position, the absence of a medial mental foramen (MMF), the mandibular canal set just below the tooth row. The occurrence of a single lateral mental foramen may represent a shared derived character of Daouitherium, Numidotherium, and Barytherium. A unique derived feature of the Elephantinae mandible is the occurrence of a medial mental foramen on the medial side of the incisive part of the mandible. MMFs have never been observed in other proboscideans excluding elephantines. The very high frequency of MMFs observed in Mammuthus meridionalis–Mammuthus trogontherii–Mammuthus primigenius (>93 per cent of the studied specimens) could be considered a synapomorphy of this group. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161 , 391–413.     

New material of Palaeoamasia kansui (Embrithopoda,Mammalia) from the Eocene of Turkey and a phylogenetic analysis of Embrithopoda at the species level

Since the discovery of the megaherbivore Arsinoitherium zitteli Beadnell (early Oligocene of Egypt), the extinct order Embrithopoda has remained an enigmatic group, with disputed affinities among ungulates. In this study, new specimens of Palaeoamasia kansui from the early Palaeogene of Turkey are described and a synthetic dental terminology is proposed for embrithopods. Based on 130 cranial–mandibular and dental characters, the first phylogenetic analysis of embrithopods is carried out in aim to enhance the position of Palaeoamasia within embrithopods. The monophyly of Embrithopoda is confirmed, following the topology (Phenacolophus (Namatherium (Arsinoitheriinae, Palaeamasiinae))). However, phylogenetic relationships between Eurasian embrithopods (Palaeoamasiinae: Palaeoamasia, Crivadiatherium and Hypsamasia) remain unresolved. The integration of all embrithopod genera within a cladistic analysis encompassing a wider taxonomic sample (Condylarthra, Afrotheria/Paenungulata and Laurasiatheria) also supports Embrithopoda as being monophyletic, but questions the position of both Phenacolophus and Namatherium within Embrithopoda. Finally, possible faunal exchange events are proposed based on three hypothesized scenarios between Eurasia and Arabia–Africa during the early Palaeogene.     

Enamel Structure of Cuvieronius hyodon (Proboscidea, Gomphotheriidae) with a Discussion on Enamel Evolution in Elephantoids

Dental material of the South American elephantoid Cuvieronius hyodon from the Late Pleistocene of the Tarija Basin, Bolivia was sampled for a comprehensive analysis of the microstructure of the enamel. To examine variability at the dentition level, enamel samples of the upper incisor, second deciduous premolar, and molars were sectioned. The incisor and cheek teeth enamel is compared to that of other proboscideans in order to reveal phylogenetically and functional informative features useful to reconstruct the evolution of elephantoid enamel. Studies of the adaptations and evolution of proboscidean enamel have focused so far on molars. Nevertheless, given the possibility of an independent evolution of the enamel at different tooth positions, the variation of the enamel throughout the dentition needs to be taken into consideration when using enamel microstructural characters to infer proboscidean diversity and phylogeny. The results obtained from this study demonstrate the generality, among elephantoids, of the basic microstructural features of Cuvieronius hyodon enamel, allowing the characterization of the Elephantoid Enamel (EE). The differentiation between incisor and molar enamel seen in elephantoids is shown to represent a primitive elephantiform trait, as it also occurs in Phiomia. The three-layered enamel of the cheek teeth appears as the sole synapomorphy of the Elephantoidea, though the character might be homoplastic within the Proboscidea. Characters of the prisms cross-section might be used, on the other hand, to define less inclusive clades within the Elephantoidea.     

A unique form of dental bilophodonty and a functional interpretation of peculiarities in the masticatory system of Arsinoitherium (mammalia,Embrithopoda)

The highly autapomorphic upper molar bilophodonty of the Oligocene mammal, Arsinoitherium (Embrithopoda) is an extreme form of dilambdodonty effected by lingual positioning of normally buccally situated cusps with reduction of lingual cusps. This effectively limits the molar dentition to a single phase shearing occlusal motion. Molar and premolar morphology is very different, premolars exhibiting high longitudinal ectolophs and typical two phase occlusal morphology. A double faceted mandibular condyle and angular discontinuity between lower molar and premolar dentitions is interpreted as a means of separating premolar from molar occlusion. A bifunctional masticatory system is proposed whereby efficient premolar occlusion is achieved only after a repositioning of the temporomandibular joint. Loss of phase II occlusion in the molars is compensated by maintenance of a crushing/grinding mode in the premolars. This coupled with the ability to maintain high occlusal pressures along the length of the mandible explains the unbroken dental arcade. Arsinoitheres therefore possess an extremely specialised masticatory apparatus and are interpreted as highly selective browsing herbivores.     

Was the Early Eocene proboscidean Numidotherium koholense semi-aquatic or terrestrial? Evidence from stable isotopes and bone histology

The Early Eocene deposits of El Kohol, Algeria, have yielded numerous remains of Numidotherium koholense, one of the most primitive and oldest known proboscideans in Africa. The Upper Eocene proboscideans of the Fayum locality (Egypt), Barytherium sp. and Moeritherium sp., were recently interpreted as aquatic or semi-aquatic, according to the stable isotopic compositions (δ¹³C and δ¹⁸O) of their tooth enamel. These data led us to reinvestigate the adaptations of N. koholense. Stable isotopic analysis and observations of histological sections of its long bones reveal that it was essentially terrestrial. According to its position within the phylogenetic tree of Eocene proboscideans, the adaptation to semi-aquatic life appears to have evolved independently in different lineages of Middle and Upper Eocene proboscideans during their adaptive radiation in Africa. Moreover, these new results reopen the debate about the hypothesis that Eocene to Recent proboscideans are derived from semi-aquatic ancestors.     

The periotic of Moeritherium (Mammalia, Proboscidea): homology or homoplasy in the ear region of Tethytheria McKenna, 1975?

The periotic of Moeritherium is described for the first time. A number of potentially autapomorphic features are identified; however, in common with living elephants and seacows the moerithere periotic is shown to lack the fenestra cochleae and aqueductus cochleae typical of therian mammals. Instead, it possesses a secondarily undivided perilymphatic foramen, a feature considered to be a synapomorphy uniting Proboscidea and Sirenia within the Tethytheria. The supposedly more derived fossil proboscidean, Mimidotherium , along with the primitive fossil sirenian Prorastomus , possess the typical therian pattern of openings to the pars cochlearis of the periotic. It is therefore unclear whether the condition in Recent tethytheres is homologous or independently derived. It is argued that the presence in Moeritherium of a suite of periotic characters more derived than those in Mimidotherium undermines the primitive status of moeritheres relative to numidotheres and all other Proboscidea, and therefore weakens the hypothesis of a secondary reversal to a more primitive auditory region in Numidotheriurn. The biological role of auditory specializations in Recent tethytheres is shown to have been very different, and it is argued that this functional disparity extends to the most primitive members of each order. Demonstrable homoplasy in structure and lack of functional congruence in basal members of both Sirenia and Proboscidea are deemed to be indicative of an independent acquisition of similar structures in the ear region of Recent tethytheres.     

The Dance of Tusks: Rediscovery of Lower Incisors in the Pan-American Proboscidean Cuvieronius hyodon Revises Incisor Evolution in Elephantimorpha

The incisors of proboscideans (tusks and tushes) are one of the most important feature in conservation, ecology and evolutionary history of these mammals. Although the absence of upper incisors is rare in proboscideans (occurring only in deinotheres), the independent losses of lower incisors are recognized for most of its lineages (dibelodont condition). The presence of lower incisors in the Pan-American gomphothere Cuvieronius hyodon was reported a few times in literature, but it was neglected in systematic studies. We analyzed several specimens of Cuvieronius hyodon from the Americas and recognized that immature individuals had lower incisors during very early post-natal developmental stages. Subsequently, these are lost and lower incisors alveoli close during later developmental stages, before maturity. Moreover, for the first time in a formal cladistic analysis of non-amebelodontine trilophodont gomphotheres, Rhynchotherium and Cuvieronius were recovered as sister-taxa. Among several non-ambiguous synapomorphies, the presence of lower incisors diagnoses this clade. We recognize that the presence of lower incisors in Cuvieronius and Rhynchotherium is an unique case of taxic atavism among the Elephantimorpha, since these structures are lost at the origin of the ingroup. The rediscovery of the lower incisors in Cuvieronius hyodon, their ontogenetic interpretation and the inclusion of this feature in a revised phylogenetic analysis of trilophodont gomphotheres brought a better understanding for the evolutionary history of these proboscideans.     

Petrosal and Bony Labyrinth Morphology Supports Paraphyly of Elephantulus Within Macroscelididae (Mammalia,Afrotheria)

Interest in the phylogeny of Macroscelididae (sengis or elephant shrews) has been prompted by molecular studies indicating that Elephantulus rozeti is best placed as the sister group of Petrodromus tetradactylus (this clade being in turn the sister taxon to Macroscelides proboscideus) than among other species of the genus Elephantulus. Until now, no discrete morphological characters have been proposed to support the grouping of E. rozeti, Petrodromus, and Macroscelides into this single so-called ‘Panelephantulus’ clade. Here, we employed μCT scanning in order to investigate the petrosal and bony labyrinth (bony capsule of the inner ear) morphology of most species of extant Macroscelididae. We performed a cladistic analysis on ear traits and found that despite some convergences (e.g., concerning the bony arterial canals in Macroscelides and Rhynchocyon) the middle and inner ear morphology furnishes significant support for the ‘Panelephantulus’ clade. In our analysis, this clade is unambigously supported by the presence of a fully ossified stapediofacial tube. Two additional characters (the presence of a bony septum at the mouth of the fenestra cochleae dividing the D3 sinus into two distinct cavities and the absence of an accessory lateral pneumatic fossa) could also support ‘Panelephantulus.’ These newly discovered morphological characters support the molecular phylogenies published and highlight the importance of coding hitherto difficult to sample morphologies within cladistic analyses using micro-CT techniques. Taxonomic implications are briefly discussed.     

The morphology of the eutherian ethmoidal region and its implications for higher‐order phylogeny

The ethmoidal region is the most rostral part of the mammalian cranium and provides the surface for the olfactory epithelium. It is part of the respiratory tract and comprises certain mechanic and mechanosensoric functions depending on the species’ mode of foraging. It is one of the least studied aspects of cranial anatomy. A complete and precise characterization of the previously undescribed fetal nasal regions of the aardvark (Orycteropus afer, Tubulidentata), the African elephant (Loxodonta africana, Proboscidea) and the rock hyrax (Procavia capensis, Hyracoidea) is given. The morphology of the ethmoidal region in O. afer and L. africana, highly macrosmatic mammals, is complicated and in many aspects derived, whereas the nasal structures in P. capensis are fairly simple. In order to contribute to current debates on higher‐order eutherian systematics 24 skeletal and soft‐tissue characters in 26 mammalian taxa (25 eutherian taxa and 1 marsupial as outgroup) were evaluated and optimized onto recent eutherian phylogenies (one morphology and one molecular based phylogeny, respectively). It is shown that the ethmoidal region is highly variable within eutherians and its structural elements display a strong tendency towards homoplasy. Therefore, this cranial region is not suitable for use in mammalian superordinal systematics except as support for monophyletic Tethytheria.     

Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements

Angular head movements in vertebrates are detected by the three semicircular canals of the inner ear and their associated sensory tissues, the cristae. Bone morphogenetic protein 4 (Bmp4), a member of the Transforming growth factor family (TGF-β), is conservatively expressed in the developing cristae in several species, including zebrafish, frog, chicken, and mouse. Using mouse models in which Bmp4 is conditionally deleted within the inner ear, as well as chicken models in which Bmp signaling is knocked down specifically in the cristae, we show that Bmp4 is essential for the formation of all three cristae and their associated canals. Our results indicate that Bmp4 does not mediate the formation of sensory hair and supporting cells within the cristae by directly regulating genes required for prosensory development in the inner ear such as Serrate1 (Jagged1 in mouse), Fgf10, and Sox2. Instead, Bmp4 most likely mediates crista formation by regulating Lmo4 and Msx1 in the sensory region and Gata3, p75Ngfr, and Lmo4 in the non-sensory region of the crista, the septum cruciatum. In the canals, Bmp2 and Dlx5 are regulated by Bmp4, either directly or indirectly. Mechanisms involved in the formation of sensory organs of the vertebrate inner ear are thought to be analogous to those regulating sensory bristle formation in Drosophila. Our results suggest that, in comparison to sensory bristles, crista formation within the inner ear requires an additional step of sensory and non-sensory fate specification.     

Taxonomy of Mechanitis (F.) (Lepidoptera: Nymphalidae) from the West Colombian Andes: an Integrative Approach

Species identification in the butterfly genus Mechanitis (F.) (Lepidoptera: Nymphalidae) becomes difficult when it is based only on wing color patterns, a common practice in butterfly taxonomy. Difficulties in Mechanitis taxonomy are related to the widespread mimicry and polymorphism among species belonging to this genus. Species recognition and inventories of Mechanitis genus in geographic areas as the Andean region of Colombia are of particular interest and the use of more than one character for taxonomic identification is desirable. In this study, we included morphological, ecological, and mitochondrial DNA data to identify the occurring species in this region. Species of Mechanitis were studied from ecological, morphological, and molecular perspectives considering host plant identification, oviposition behavior, and life cycles under laboratory conditions. Immature morphology, patterns of wing color, and genital structures of adults were also studied. The genetic barcoding region of the cytochrome oxidase I mitochondrial gene was sequenced and used to verify the limits between species previously defined by the other characters and to validate its usefulness for species delimitation in this particular genus. The integrative approach combining independent datasets successfully allowed species identification as compared to the approach based on a single dataset. Three well-differentiated species were found in the studied region, Mechanitis menapis (Hewitson), Mechanitis polymnia (Linnaeus), and Mechanitis lysimnia (Fabricius). New valuable characters that could improve taxonomic identification in this genus are considered.     

The first described Arsinoitherium from the upper Eocene Aydim Formation of Oman: Biogeographic implications

A new fossiliferous locality is discovered from the upper Eocene Aydim Formation, in Dhofar, Southern Sultanate of Oman. A left ulna of Arsinoitherium is described, and cranial and postcranial specimens found in close proximity are referred to the same taxon. The locality is promising for the recovery of additional fossil specimens. Moreover, the presence of Arsinoitherium in Oman is of biogeographic significance; as the Red Sea did not exist during the late Eocene, these large-bodied animals were able to freely travel between what is now the Arabian Peninsula and continental Africa.