Evolutionary origins of ultrasonic hearing and laryngeal echolocation in bats inferred from morphological analyses of the inner ear

PMCID: PMC3598973This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited

Digital reconstruction of the inner ear of Leptictidium auderiense (Leptictida, Mammalia) and North American leptictids reveals new insight into leptictidan locomotor agility

Leptictida are basal Paleocene to Oligocene eutherians from Europe and North America comprising species with highly specialized postcranial features including elongated hind limbs. Among them, the European Leptictidium was probably a bipedal runner or jumper. Because the semicircular canals of the inner ear are involved in detecting angular acceleration of the head, their morphometry can be used as a proxy to elucidate the agility in fossil mammals. Here we provide the first insight into inner ear anatomy and morphometry of Leptictida based on high-resolution computed tomography of a new specimen of Leptictidium auderiense from the middle Eocene Messel Pit (Germany) and specimens of the North American Leptictis and Palaeictops. The general morphology of the bony labyrinth reveals several plesiomorphic mammalian features, such as a secondary crus commune. Leptictidium is derived from the leptictidan groundplan in lacking the secondary bony lamina and having proportionally larger semicircular canals than the leptictids under study. Our estimations reveal that Leptictidium was a very agile animal with agility score values (4.6 and 5.5, respectively) comparable to Macroscelidea and extant bipedal saltatory placentals. Leptictis and Palaeictops have lower agility scores (3.4 to 4.1), which correspond to the more generalized types of locomotion (e.g., terrestrial, cursorial) of most extant mammals. In contrast, the angular velocity magnitude predicted from semicircular canal angles supports a conflicting pattern of agility among leptictidans, but the significance of these differences might be challenged when more is known about intraspecific variation and the pattern of semicircular canal angles in non-primate mammals

The petrosal bone and inner ear of Micromeryx flourensianus (Artiodactyla, Moschidae) and inferred potential for ruminant phylogenetics

While petrosal bones have a long research history in artiodactyl phylogenetics, the inner ear embedded in this bone has rarely been investigated. I describe here a set of petrosals and the associated inner ears of the Middle Miocene moschid Micromeryx flourensianus from the German locality Steinheim and compare them to the extant musk deer Moschus moschiferus (Moschidae), the four-horned antelope Tetracerus quadricornis (Bovidae) and the white-tailed deer Odocoileus virginianus (Cervidae). Inner ears were reconstructed using high resolution x-ray computed tomography scans. In phylogenenetic reconstructions built on morphological and molecular data, Moschidae has variously been shown to be a sister taxon to Bovidae or Cervidae. Its position hasn’t reached a consensus yet. Studying the inner ear morphology adds new morphological characters that will help resolving this question. Micromeryx flourensianus is an abundant fossil moschid and I show indeed that its petrosal bone and inner ear share several similarities with that of the extant musk deer such as a ventral basicapsular groove, a well-developed anterior process of the tegmen tympani, or a fossa for the tensor tympani muscle in the musk-deer that may well have evolved from a Micromeryx-like condition. Inner ears share a thick basal cochlear whorl, a bulky vestibule, or a short and thick cochlear aqueduct. This shows that inner ears have a high potential for taxonomy and phylogenetics. Including the inner ear of a fossil skull of Micromeryx flourensianus also from Steinheim, four inner ears are described here and give insights into the morphological variability of this structure at an intraspecific level as well as into the post-natal ontogenetic changes that occur. This contribution is a first step towards a comprehensive understanding of the evolution of the ruminant inner ear

Craniodental Adaptation and Homoplasy in Early Mammals

For the first two-thirds of their over 180-million-year history, mammals left a sparse fossil record. Often the only direct evidence of these early forms are small and unassociated craniodental fragments. Despite these limitations, the three chapters of this thesis support the effectiveness of this type of material for estimating the functional and autecological capacities in Mesozoic mammals, through high resolution imaging and morphometric analysis of the molariform dentition. Each of the three chapters is a self-contained study addressing separate topics relating to the evolution of dental and petrosal morphology. The common thread between all sections is that variation in craniodental structure among Mesozoic lineages is greater than would be expected based only on the disparity seen among extant small mammals. This is a result of both the more “modern” dynamics of dental evolution in more Mesozoic mammalian lineages than historically appreciated (Chapters 1 and 3), and the more “primitive” morphology of the inner ear, even in groups very closely related to extant crown therians (Chapter 2). In both cases, the craniodental morphologies described are outside the range of variation seen in extant species. Chapter 1 describes several new specimens from the herbivorous stem-therian mammal Reigitherium, from the Late Cretaceous of Patagonia. These newly available specimens demonstrate that the herbivorous molar morphology seen in Reigitherium is derived from the more plesiomorphic tuberculosectorial pattern seen in the South American endemic group Meridiolestida. Chapter 2 presents descriptions and analysis of the internal structure of three stem therian petrosal bones from the Late Jurassic of North America, and middle Cretaceous of Mongolia. Within the comparative context of labyrinthine endocast evolution, it can be determined that many of the advanced features of modern therian hearing likely developed only after their divergence from their common ancestor with the fossil groups described here. Finally, Chapter 3 presents a macroevolutionary analysis of lower molariform shape change across a large sample of early mammaliaforms, using high-level morphometric methods. The results of this analysis suggest that the stochastic processes controlling the shape evolution of lower molariforms in crown Mammalia are shared across a wide range of “triconodont”, “symmetrodont”, and “tribosphenic” Mesozoic taxa

A new close mammal relative and the origin and evolution of the mammalian central nervous system

Mammals are distinguished by the presences of the cerebral neocortex, and dentary-squamosal jaw joint, among other traits. These traits likely evolved outside of Mammalia, in Mammaliaformes. Recent fossil discoveries from South America elucidate the evolution of the brain in taxa outside of Mammaliaformes. A new skull of a close mammal relative, Pseudotherium argentinus, from the Late Triassic Ischigualasto Formation in Argentina was scanned at The University of Texas High-Resolution X-ray Computed Tomography (CT) Facility. CT data reveal a unique combination of ancestral and derived characters. Phylogenetic analysis supports a sister-taxon relationship between Pseudotherium and the derived Tritylodontidae. An endocast reconstruction further supports a derived phylogenetic position among cynodonts. A comparison of the Pseudotherium endocast with other cynodont endocasts suggests that the cerebral hemispheres enlarged in probainognathian cynodonts, while the total endocranial volume remained relatively constant until the origin of Mammaliaformes. This expansion is also present in the foramen magnum. Encephalization volume and skull length were compared with foramen magnum size in extinct and extant cynodonts, birds, and lizards. Endocranial volume and foramen magnum size, and foramen magnum size and skull length, are correlated following a 3/2 power law. Therefore, foramen magnum size can be used to predict endocranial volume for fossils. Regression analyses show foramen magnum size is significantly increased in Mammaliaformes. This change reflects an increase in medulla oblongata size and supports a concerted model of brain evolution outside of Mammalia. Because the increase in medullary size coincides with the origin of the neocortex, I hypothesize that the mammalian pyramidal tract originated in Mammaliaformes. The hypotheses from this dissertation are testable given recent fossil discoveries. However, morphological data of those specimens are not readily available. Morphological descriptions in this dissertation are accompanied by detailed figures, and the data will be digitally archived and made publically available on DigiMorph.org. The intent is to model a communication and data-sharing standard to be implemented in all future fossil discoveries.Geological Science

Morphology of the petrosal and stapes of Borealestes (Mammaliaformes, Docodonta) from the Middle Jurassic of Skye, Scotland

We describe, in unprecedented detail, the petros-als and stapes of the docodont Borealestes from the Middle Jurassic of Scotland, using high resolution lCT and phase- contrast synchrotron imaging. We describe the inner ear endocast and the vascularized interior structure of the pet-rosal, and provide the first endocranial view of a docodontan petrosal. Our study confirms some similarities in petrosal and stapedial morphology with the better known Haldan-odon of the Late Jurassic of Portugal, including: (1) the degree of curvature of the cochlea; (2) multiple features related to the highly pneumatized paroccipital region; (3) the shape of lateral trough, the fossa of the M. tensor tym-pani, and the ridge on the promontorium; (4) the round shape of the fenestra vestibuli; and (5) overall morphology of the stapes. But Borealestes differs from Haldanodon in having a bony ridge that separates the tympanic opening of the prootic canal, the secondary facial foramen and the hia-tus Fallopii, from the fenestra vestibuli. We identify two new vascular structures: the anterior and posterior trans-cochlear sinuses, which traverse the pars cochlearis around the cochlear nerve (VIII). These trans-cochlear sinuses have not been observed in previous docodont specimens, and could be an autapomorphy of Borealestes, or apomorphic for this clade. We also establish the anatomical relationship of the circum-promontorium plexus to the inner endocast. The high quality of our scans has made these structures visible for the first time

Craniodental anatomy in Permian-Jurassic Cynodontia and Mammaliaformes (Synapsida, Therapsida) as a gateway to defining mammalian soft tissue and behavioural traits

Mammals are diagnosed by more than 30 osteological characters (e.g. squamosal-dentary jaw joint, three inner ear ossicles, etc.) that are readily preserved in the fossil record. However, it is the suite of physiological, soft tissue and behavioural characters (e.g. endothermy, hair, lactation, isocortex and parental care), the evolutionary origins of which have eluded scholars for decades, that most prominently distinguishes living mammals from other amniotes. Here, we review recent works that illustrate how evolutionary changes concentrated in the cranial and dental morphology of mammalian ancestors, the Permian-Jurassic Cynodontia and Mammaliaformes, can potentially be used to document the origin of some of the most crucial defining features of mammals. We discuss how these soft tissue and behavioural traits are highly integrated, and how their evolution is intermingled with that of craniodental traits, thus enabling the tracing of their previously out-of-reach phylogenetic history. Most of these osteological and dental proxies, such as the maxillary canal, bony labyrinth and dental replacement only recently became more easily accessible - thanks, in large part, to the widespread use of X-ray microtomography scanning in palaeontology - because they are linked to internal cranial characters. This article is part of the theme issue 'The mammalian skull: development, structure and function'.Fil: Norton, Luke A.. University of the Witwatersrand; SudáfricaFil: Abdala, Nestor Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; Argentina. University of the Witwatersrand; SudáfricaFil: Benoit, Julien. University of the Witwatersrand; Sudáfric