Evolutionary analysis of the middle and inner ear of Late Jurassic multituberculates

We describe three previously unreported specimens of petrosal bones of paulchoffatiid multituberculate mammals, collected from strata of Late Jurassic age in the Guimarota lignite mine of Leiria, west-central Portugal. The new fossils allow correction, supplementation, and confirmation of anatomical details, thus refining knowledge of general adaptation in the ear region among Jurassic multituberculates. Virtually all observed characters in the paulchoffatiid otic region are primitive relative to homologous features seen among Late Cretaceous and younger representatives of the Multituberculata; we recognize few unique otic specializations in paulchoffatiids that would preclude ancestry to later multituberculates. The plesiomorphic nature of paulchoffatiid ear regions provides no evidence in support of the hypothesis of a special, sister-group relationship between multituberculates and Late Cretaceous/Cenozoic marsupials plus placentals. Used in isolation, objective evidence derived from paulchoffatiid ear regions is consistent with interpretation of multituberculate divergence from other mammals predating the stem to living monotremes and postdating the stem to extinct morganucodontids. More broadly based comparative studies among Mesozoic mammals, however, suggest that independent acquisition of similarly advanced mammalian features was a pervasive theme among evolutionary histories of early mammals, probably including multituberculates. Although the phylogenetic position of multituberculates relative to other mammalian groups has yet to be unequivocally resolved, we suggest that a very early divergence of the group remains a distinct possibility.     

An X-radiographic and SEM study of the osseous inner ear of multituberculates and monotremes (Mammalia): implications for mammalian phylogeny and evolution of hearing

Multituberculate petrosals with well-preserved, three-dimensional internal anatomy from the Late Cretaceous/early Paleocene Bug Creek Anthills, Montana, U.S.A., are described from X-radiographic and SEM images, as well as from conventional visual observations, and are compared with the anatomy of the osseous inner ear in monotremes and in primitive non-therian and therian mammals. Results of this study indicate that: (1) the cochlea of at least some multituberculates retained a lagena, previously known only in monotremes among mammals; (2) an enlarged vestibule evolved in several lineages of multituberculates independently, and hence is not a synapomorphy of the order; (3) the cochlear canal lacks osseous laminae in support of the short, wide basilar membrane, which was probably inefficient in responding to high-frequency airborne vibrations; and (4) consequently, bone-conducted hearing in some multituberculate species may have been important in interpretation of their surroundings. Comparisons with the inner ear of monotremes and primitive therians indicate that curvature of the cochlea and cribriform plates for passage of vestibulocochlear nerve branches through the petrosal are unlikely homologues between monotremes and therians. From non-therian to therian mammals, there is a distinct morphological gap in the inner ear transition, characterized by acquisition of a number of neomorphs in the therian inner ear; an intermediate stage has yet to be discovered.     

Characters of multituberculates neglected in phylogenetic analyses of early mammals

Multituberculate anatomy is compared with that of other mammals, with an emphasis on the characters that have either been neglected or misinterpreted in previous analyses of early mam mal relationships. These are: brain structure, backward masticatory power stroke (along with aspects of cranial design), and foot structure. New data on ear ossicles and a controversy con cerning multituberculate posture are also discussed. The following characters of multitubercu late skull and lower jaw are interpreted to be related to the backward masticatory power stroke: anterior orbital area roofed dorsally and without a floor (characteristic of advanced multituber culates), parietal postorbital process, lack of the angular process and a more anterior position of the coronoid process and masseteric fossa than in all other mammals. It is argued that the parallel development in the cranial structure of multituberculates and other mammals was lim ited by the backward masticatory power stroke of multituberculates that resulted in different configuration of the masticatory musculature and related osteology. In the postcranial skeleton the parallelism was limited by the structure of the multituberculate foot, in which the calca-neum contacts the fifth metatarsal (MtV) and the middle metatarsal (MtIII) is abducted 30° from the longitudinal axis of the tuber calcanei. Backward masticatory power stroke and related skull design do not show unequivocally whether multituberculates originated from some ‘tri-conodonts’ (a polyphyletic group), or independently from all other mammals from cynodonts. The foot structure refutes the origin of multituberculates from the Morganucodontidae. The brain structure allies the multituberculates with the Triconodontidae, the postcranial skeleton of which remains unknown. New data on ear ossicles suggest close relationships of multituber culates to all modern mammals. Lack of uncontested pre-Kimmeridgian multituberculates dis proves the separate origin of multituberculates from cynodonts.     

The Inner Ear of Two Late Cretaceous Multituberculate Mammals, and Its Implications for Multituberculate Hearing

The inner ear of the Late Cretaceous multituberculates Nemegtbaatar gobiensis and Chulsan-baatar vulgaris is described from serial sections and enlarged models. The size and proportions of the inner ear as a whole are as expected for extant small mammals. The lengths of the cochlea (Nemegtbaatar gobiensis, 3.0 mm, Chulsanbaatar vulgaris, 2.0 mm) are comparable to those of other multituberculates, when ratios of length of the cochlea to skull length are calculated. The vestibule is not as expanded in the two taxa as in Lambdopsalis, ?Meniscoessus, and ?Catopsalis; the estimated volume for Nemegtbaatar gobiensis is 9 mm³. A slightly laterally curved, anteriomedially directed cochlea, relatively robust ear ossicles, and the estimations of the area of the tympanic membrane and stapedial footplate in Chulsanbaatar suggest high-frequency hearing but a relatively low sensitivity to low-decibel sounds. The semicircular canals of Nemegtbaatar and Chulsanbaatar are fully developed; the size of the anterior, posterior, and lateral canals and their angles and proportions are comparable to those of extant mammals of similar size. The anterior semicircular canal of Nemegtbaatar forms a smooth half-circle and thus is more derived than the angular canal of Ornithorhynchus. The notable differences between the ratio of the width of the lateral semicircular canal to skull length and the size of the vestibule in Nemegtbaatar and the Paleocene multituberculate Lambdopsalis bulla are probably related to different modes of life.     

虔州豫俊兽(Yubaatarqianzhouensissp.nov.):江西赣州盆地首例晚白垩世哺乳动物化石*

本文报道了产自江西省赣州市上白垩统赣县河口组的一件多瘤齿兽类标本, 这是江西省报道的首例中生代哺乳动物化石。此标本头骨后部横向扩展, 额骨较小, 后端尖并构成眼眶的内侧边缘, M1具三列齿尖, 系统发育分析支持其归入纹齿兽超科。与河南晚白垩世的中原豫俊兽形态较为相似, 但是两者间也存在一些明显的区别, 因此建立一个豫俊兽属新种——虔州豫俊兽(Yubaatar qianzhouensis sp. nov.), 鉴定特征为: m1齿尖式为7︰6; M2齿尖式为1︰3︰3; m1颊侧后部存在一道小脊; 虔州豫俊兽m2和m1的长度比例小于中原豫俊兽; 冠状突呈楔状, 末端尖。虔州豫俊兽的发现不仅扩展了晚白垩世多瘤齿兽类在东亚地区的地理分布和物种多样性, 并且也扩展了中生代哺乳动物的地理分布。     

A NEW NEOPLAGIAULACID MULTITUBERCULATE (MAMMALIA) FROM THE LOWER EOCENE OF WUTU BASIN, SHANDONG

TheWutuspecimenswerecol1ectedfromWutuFormation,LowerEoceneinl992andareconcurrentwithChangleIestcsdissetiformis(Insectivora,seeTongandWang,l993),ischyromyidrodents,carpo1estidprimates,primitiveperissodactylsandothermammals.MultituberculataCope,l884PtilodontoideaSloanandVanValen,l965NeoplagiauladdaeAmeghino,189oMesodmopsdaw8onaegen.etsp.nov.(Text-fig.l-2,Pl.l,II)TypeAfragmentaryskullwithrightdP1-M2andleftdP'-M',anear1ycompleterightmandiblewithI,andP'-M,,anincompleteleftmandiblewithP.…     

The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration?

The inner ear of mammals uses neurosensory cells derived from the embryonic ear for mechanoelectric transduction of vestibular and auditory stimuli (the hair cells) and conducts this information to the brain via sensory neurons. As with most other neurons of mammals, lost hair cells and sensory neurons are not spontaneously replaced and result instead in age-dependent progressive hearing loss. We review the molecular basis of neurosensory development in the mouse ear to provide a blueprint for possible enhancement of therapeutically useful transformation of stem cells into lost neurosensory cells. We identify several readily available adult sources of stem cells that express, like the ectoderm-derived ear, genes known to be essential for ear development. Use of these stem cells combined with molecular insights into neurosensory cell specification and proliferation regulation of the ear, might allow for neurosensory regeneration of mammalian ears in the near future.     

A Systematic Study on Tooth Enamel Microstructures of Lambdopsalis bulla (Multituberculate,Mammalia) - Implications for Multituberculate Biology and Phylogeny

Tooth enamel microstructure is a reliable and widely used indicator of dietary interpretations and data for phylogenetic reconstruction, if all levels of variability are investigated. It is usually difficult to have a thorough examination at all levels of enamel structures for any mammals, especially for the early mammals, which are commonly represented by sparse specimens. Because of the random preservation of specimens, enamel microstructures from different teeth in various species are often compared. There are few examples that convincingly show intraspecific variation of tooth enamel microstructure in full dentition of a species, including multituberculates. Here we present a systematic survey of tooth enamel microstructures of Lambdopsalis bulla, a taeniolabidoid multituberculate from the Late Paleocene Nomogen Formation, Inner Mongolia. We examined enamel structures at all hierarchical levels. The samples are treated differently in section orientations and acid preparation and examined using different imaging methods. The results show that, except for preparation artifacts, the crystallites, enamel types, Schmelzmuster and dentition types of Lambdopsalis are relatively consistent in all permanent teeth, but the prism type, including the prism shape, size and density, may vary in different portions of a single tooth or among different teeth of an individual animal. The most common Schmelzmuster of the permanent teeth in Lambdopsalis is a combination of radial enamel in the inner and middle layers, aprismatic enamel in the outer layer, and irregular decussations in tooth crown area with great curvature. The prism seam is another comparably stable characteristic that may be a useful feature for multituberculate taxonomy. The systematic documentation of enamel structures in Lambdopsalis may be generalized for the enamel microstructure study, and thus for taxonomy and phylogenetic reconstruction, of multituberculates and even informative for the enamel study of other early mammals.     

What did Morganucodon hear?

The structure of the middle and inner ear of Morganucodon , one of the oldest known mammals, is reviewed and compared to the structure of the ears of extant mammals, reptiles and birds with known auditory capabilities. Specifically, allometric relationships between ear dimensions (basilar-membrane length, tympanic-membrane area and stapes-footplate area) and specific features of the audiogram are defined in extant ears. These relationships are then used to make several predictions of auditory function in Morganucodon. The results point out that the ear structures of Morganucodon–Art similar in dimensions to ear structures in both extant small mammals–with predominantly high-frequency (10 kHz) auditory capabilities, and reptiles and birds- with better low and middle-frequency hearing (< 5 kHz). Although the allometric analysis cannot by itself determine whether Morganucodon heard more like present-day small mammals, or birds and reptiles, the apparent stiffness of the Morganucodon middle ear is both more consistent with the high-frequency mammalian middle ear and would act to decrease the sensitivity of a bird-reptile middle ear to low-frequency sound. Several likely hearing scenarios for Morganucodon are defined, including a scenario in which these animals had ears like those of modern small mammals that are selectively sensitive to high-frequency sounds, and a second scenario in which the Morganucodon ear was moderately sensitive to sounds of a narrow middle-frequency range (5–7 kHz) and relatively insensitive to sounds of higher or lower frequency. The evidence needed to substantiate either scenario includes some objective measure of the stiffness of the Morganucodon ossicular system, while a key datum needed to distinguish between the two hypotheses includes confirmation of the presence or absence of a cochlear lamina in the Morganucodon inner ear.     

Book Review

Book Reviewed in this article:
K ielan -J aworowska , J.; G ambaryan , P. P.: Posteranial anatomy and habits of Asian multituberculate mammals .     

Planar polarity in mammals: similarity and divergence with Drosophila Melanosgaster

Planar cell polarity (PCP) genes were originally identified in invertebrates (Drosophila Melanogaster) for their role in the uniform orientation of a structure within the plane of the epithelium (hair, group of cells). During the last five years, numerous studies have shown that vertebrate, but more importantly, mammalian homologues of some of these genes are involved in various developmental processes such as neural tube closure, polycystic kidney disease, inner ear functions (hearing, balance) or Bardet Biedl syndrome. These processes rely on a set of genes whose PCP function is conserved in mammals and Drosophila Melanogaster for some, or only present in mammals for others. In 2003, the inner ear was identified as a model to study PP in mammals and allowed the identification of the first important genes. These genes encode a variety of cell surface molecules as well as intracellular adapters whose molecular mechanisms are still poorly understood. It is clear that the identification of the PP pathways in mammals will come from a comparison with the genes in Drosophila, but also from the identification of genes specific to mammals.     

Preliminary observations on the morphology of the inner ear of the fetal narwhal (Monodon monoceros)

The inner ear of the narwhal (Monodon monoceros) was investigated on the basis of a complete series of microslides of an early fetus. In this well‐preserved specimen, the cochlea is about twice as large as the vestibular apparatus. The latter exhibits a high degree of specialization. Whereas the utriculus and sacculus are of normal size in comparison with those of other mammals, the semicircular canals are miniaturized but not obliterated, as in the case of some adult toothed whales. In comparison with other mammals, there is relatively little perilymphatic space around the vestibular organ, but the inner radius of the lymphatic ducts comes close to that of the adult human. Although there are some hints that the sensitivity of the vestibular system may be high in this species, detailed analysis of the adult narwhal ear is needed to confirm this inference.     

Patterning and morphogenesis of the vertebrate inner ear

The positional cues for formation of individual inner ear components are dependent on pre-established axial information conferred by inductive signals from tissues surrounding the developing inner ear. This review summarizes some of the known molecular pathways involved in establishing the three axes of the inner ear, anterior-posterior (AP), dorsal-ventral (DV) and medial-lateral (ML). Signals required to establish the AP axis of the inner ear are not known, but they do not appear to be derived from the hindbrain. In contrast, the hindbrain is essential for establishing the DV axis of the inner ear by providing inductive signals such as Wnts and Sonic hedgehog. Signaling from the hindbrain is also required for the formation of the ML axis, whereas formation of the lateral wall of the otocyst may be a result of first establishing both the AP and DV axes. In addition, this review addresses how genes induced within the otic epithelium as a result of axial specification continue to mediate inner ear morphogenesis.     

Convergence vs. Specialization in the ear region of moles (mammalia)

We investigated if and how the inner ear region undergoes similar adaptations in small, fossorial, insectivoran‐grade mammals, and found a variety of inner ear phenotypes. In our sample, afrotherian moles (Chrysochloridae) and the marsupial Notoryctes differ from most other burrowing mammals in their relatively short radii of semicircular canal curvature; chrysochlorids and fossorial talpids share a relatively long interampullar width. Chrysochlorids are unique in showing a highly coiled cochlea with nearly four turns. Extensive cochlear coiling may reflect their greater ecological dependence on low frequency auditory cues compared to talpids, tenrecids, and the marsupial Notoryctes. Correspondingly, the lack of such extensive coiling in the inner ear of other fossorial species may indicate a greater reliance on other senses to enable their fossorial lifestyle, such as tactile sensation from vibrissae and Eimer's organs. The reliance of chrysochlorids on sound is evident in the high degree of coiling and in the diversity of its mallear types, and may help explain the lack of any semiaquatic members of that group. The simplest mallear types among chrysochlorids are not present in the basal‐most members of that clade, but all extant chrysochlorids investigated to date exhibit extensive cochlear coiling. The chrysochlorid ear region thus exhibits mosaic evolution; our data suggest that extensive coiling evolved in chrysochlorids prior to and independently of diversification in middle ear ossicle size and shape. J. Morphol. 276:900–914, 2015. © 2015 Wiley Periodicals, Inc.     

The ear in subterranean insectivora and rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear.

Compared to acoustically unspecialized mammals (soricids and murids), the middle ear of subterranean insectivores and rodents (twelve species of six families examined) was clearly distinguished and characterized by many common features: rather round and relatively larger eardrum without a pars flaccida; reduced gonial; loose or no connection between the malleus and the tympanic bone; reduced and straightened transversal part of the malleus; enlarged incus; increased and rather flat incudo-mallear joint; rather parallel position of the mallear manubrium and incudal crus longum in some species (and their fusion in bathyergids); reduced or even missing middle ear muscles. Convergent occurrence of these structural features in taxa of different origin and their generally derived character suggest that they cannot be categorized as degenerative. The form of the stapes can be considered as a non-adaptive trait; it was taxon specific yet remarkably polymorphous in some species and exhibited no convergent features among subterranean mammals. Structural retrogression resulting in a columella-like stapes was observed in some species lacking the stapedial artery. The stapedial base was relatively larger than in unspecialized mammals. The subterranean mammals did not exhibit conspicuously enlarged eardrums as would be required for sensitive tuning to low frequencies. It is, however, argued that while selective pressures in the subterranean ecotope promoted hearing of low frequencies, hearing sensitivity did not have to be enhanced.     

Pluripotent stem cells from the adult mouse inner ear

In mammals, the permanence of acquired hearing loss is mostly due to the incapacity of the cochlea to replace lost mechanoreceptor cells, or hair cells. In contrast, damaged vestibular organs can generate new hair cells, albeit in limited numbers. Here we show that the adult utricular sensory epithelium contains cells that display the characteristic features of stem cells. These inner ear stem cells have the capacity for self-renewal, and form spheres that express marker genes of the developing inner ear and the nervous system. Inner ear stem cells are pluripotent and can give rise to a variety of cell types in vitro and in vivo, including cells representative of ectodermal, endodermal and mesodermal lineages. Our observation that these stem cells are capable of differentiating into hair cell-like cells implies a possible use of such cells for the replacement of lost inner-ear sensory cells.     

The Phylogenetic Affinities of the Enigmatic Mammalian Clade Gondwanatheria

Gondwanatheria is a group of extinct mammals known from the Cretaceous and Paleogene of Gondwana. Resolution of the phylogenetic affinities of gondwanatherians has proven problematical, with the group currently considered Mammalia incertae sedis. We briefly review the morphology of known gondwanatherians, and argue that isolated upper premolars and a partial dentary preserving a blade-like p4 originally referred to the ferugliotheriid gondwanatherian Ferugliotherium windhauseni but subsequently identified as Multituberculata incertae sedis do indeed belong to F. windhauseni. We also suggest that the recently described ?cimolodontan multituberculate Argentodites coloniensis, based on an isolated lower premolar, may in fact be an unworn p4 of Ferugliotherium or a closely related taxon. We present the first phylogenetic analyses to include gondwanatherians, using maximum parsimony and Bayesian methods. Both methods place Ferugliotherium and sudamericid gondwanatherians in a clade with cimolodontan and “plagiaulacidan” multituberculates, although relationships within this clade are largely unresolved. The Gondwanatheria + Multituberculata clade supported here may reflect the convergent evolution of similar dental features, but it is the best supported hypothesis based on currently available data. However, denser sampling of multituberculate taxa and the discovery of more complete gondwanatherian fossils will be required to clarify the precise relationship between gondwanatherians and multituberculates, specifically to determine whether or not gondwanatherians are members of Multituberculata. We hypothesize that the anterior molariforms of sudamericid gondwanatherians evolved from blade-like precursors similar to the p4 of Ferugliotherium, possibly in response to the appearance of grasses in Gondwana during the Cretaceous.     

The ear region of Latimeria chalumnae: functional and evolutionary implications

The anatomy of Latimeria chalumnae has figured prominently in discussions about tetrapod origins. While the gross anatomy of Latimeria is well documented, relatively little is known about its otic anatomy and ontogeny. To examine the inner ear and the otoccipital part of the cranium, a serial-sectioned juvenile coelacanth was studied in detail and a three-dimensional reconstruction was made. The ear of Latimeria shows a derived condition compared to other basal sarcopterygians in having a connection between left and right labyrinths. This canalis communicans is perilymphatic in nature and originates at the transition point of the saccule and the lagena deep in the inner ear, where a peculiar sense end organ can be found. In most gnathostomes the inner ears are clearly separated from each other. A connection occurs in some fishes, e.g. within the Ostariophysi. In the sarcopterygian lineage no connections between the inner ears are known except in the Actinistia. Some fossil actinistians show a posteriorly directed duct lying between the foramen magnum and the notochordal canal, similar to the condition in the ear of Latimeria, so this derived character complex probably developed early in actinistian history. Because some features of the inner ear of Latimeria have been described as having tetrapod affinities, the problem of hearing and the anatomy of the otical complex in the living coelacanth has been closely connected to the question of early tetrapod evolution. It was assumed in the past that the structure found in Latimeria could exemplify a transitional stage in otic evolution between the fishlike sarcopterygians and the first tetrapods in a functional or even phylogenetic way. Here the possibility is considered that the canalis communicans does not possess any auditory function but rather is involved in sensing pressure changes during movements involving the intracranial joint. Earlier hypotheses of a putative tympanic ear are refuted.     

Prism Size in Tooth Enamel of Some Late Cretaceous Mammals and Its Value in Multituberculate Taxonomy

Teeth from specified members of the two suborders of Late Cretaceous Multituberculata and two Late Cretaceous therians were studied. The enamel was prismatic on all teeth. In the therian representatives and the representatives of the suborder Ptilodontoidea of the Multituberculata, the prism diameters and densities per unit area were similar to those of recent mammals. In the representatives of the suborder Taeniolabidoidea the prisms were very large and their density per unit area was 5 to 8 times lower than in recent mammals. It is suggested that gigantoprismatic enamel is a characteristic of Taeniolabidoidea and could be used as a taxonomic criterion in multituberculate systematics.