Braincase,palatoquadrate and ear region of the plagiosaurid Gerrothorax pulcherrimus from the Middle Triassic of Germany

Abstract: The complete neurocranium plus palatoquadrate of the plagiosaurid temnospondyl Gerrothorax pulcherrimus from the Middle Triassic of Germany is described for the first time, based on outer morphological observations and micro‐CT scanning. The exoccipitals are strong elements with paroccipital processes and well‐separated occipital condyles. Anterolaterally, the exoccipitals contact the otics, which are mediolaterally elongated and have massive lateral walls. The otics contact the basisphenoid, which shows well‐developed sellar processes. Anteriorly, the basisphenoid is continuous with the sphenethmoid region. In its posterior portion, the sphenethmoid gives rise to robust, laterally directed laterosphenoid walls, a unique morphology among basal tetrapods. The palatoquadrate is extensively ossified. The quadrate portion overlaps the descending lamina of squamosal and ascending lamina of pterygoid anteriorly, almost contacting the epipterygoid laterally. The epipterygoid is a complex element and may be co‐ossified with otics and laterosphenoid walls. It has a broad, sheet‐like footplate and a horizontally aligned ascending process that contacts the laterosphenoid walls. The degree of ossification of the epipterygoid, however, is subject to individual variation obviously independent from ontogenetic changes. The stapes of Gerrothorax is a large, blade‐like element that differs conspicuously from the plesiomorphic temnospondyl condition. It has a prominent anterolateral projection which has not been observed in other basal tetrapods. Morphology of neurocranium and palatoquadratum of Gerrothorax most closely resembles that of the Russian plagiosaurid Plagiosternum danilovi, although the elements are less ossified in the latter. The extensive endocranial ossification of Gerrothorax is consistent with the general high degree of ossification in the exo‐ and endoskeleton of this temnospondyl and supports the view that a strong endocranial ossification cannot be evaluated as a plesiomorphic character in basal tetrapods.     

The tail of Microbrachis (Tetrapoda; Microsauria)

Previously undescribed specimens of the aquatic microsaur Microbrachis pelikani Fritsch from the Upper Carboniferous of Nýřany, Czech Republic, demonstrate the presence of a deep-swimming-adapted tail supported by up to 46 postsacral vertebrae. The tail appears to have lengthened with ontogeny. Most microsaurs appear to have been terrestrial and because the group has been perceived to be related to the amniotes, all (including Microbrachis ) had been reconstructed with slender tapering tails. Microbrachis appears to be an early offshoot of the microsaurs and it is unclear whether the deep tail is a primitive retention or an acquired characteristic of the genus.     

Evolution of the tetrapod ear: an analysis and reinterpretation

The dominant view of tetrapod otic evolution–the “standard view”–holds that the tympanum developed very early in tetrapod history and is homologous in all tetrapods and that the opercular process of the rhipidistian hyomandibula is homologous to the tympanic process of the stapes in lower tetrapods. Under that view, the labyrinthodont amphibians of the Paleozoic are usually considered ancestral to reptiles, and thus the “otic notch” of labyrinthodonts and the tympanum it presumably contained form the starting-point for middle ear evolution in reptiles. Four problems have classically been identified with the standard view: the differing relationships of the internal mandibular branch of N. VII (chorda tympani) to the processes of the stapes in amniotes and anurans; the differing orientations of the stapes in key fossil and living groups; the location of the tympanum in early fossil reptiles; and the transferral of the tympanum, during the origin of mammals, from the stapes to the articular bone of the lower jaw. An examination of these problems and of the solutions proposed under the standard view reveals the ad hoc, and therefore unsatisfactory, nature of the proposed solutions. To organize and review alternative hypotheses of otic evolution an analytical table is constructed, using three characters (tympanic process, Nerve VII, tympanum), each with two possible states. A total of eight hypotheses about middle ear evolution are possible under this system, one of which is the standard view. The seven “non-standard” hypotheses, only five of which have been argued in the literature, are briefly examined. Six of the “non-standard” hypotheses appear unattractive for various reasons, including reliance on ad hoc arguments. The seventh was first proposed by Gaupp in 1898. It is today almost universally ignored but apparently largely for historical rather than scientific reasons. This hypothesis, her called the “alternative view”, appears to rest on assumptions equally as plausible as those of the standard view. Moreover, it offers a solution of the problems associated with the standard view without, apparently, raising any similarly serious problems. This paper compares the standard and alternative views of middle ear evolution in detail. Comparison proceeds on two levels. On one level, they are compared in terms of the hypotheses of phyletic tetrapod relationships each promotes and how strongly each supports its hypothesis. Both views promote the same hypothesis of tetrapod relationships. The alternative view is the more parsimonious, but the difference is not considered sufficient to provide a choice. On another level, the two views are compared in terms of their implications for: (1) the evolution of relative and absolute auditory perceptive ability; (2) the origin of reptiles; (3) the evolution of the suspensorium and cranial kinesis; and (4) the origin and evolution of recent amphibians. The nature of the data required for a test of the implications of the two views is specified in each case. Where data are available. the alternative view is consistent and the standard view is inconsistent with these data. We conclude that the alternative view is the preferable hypothesis of middle-ear evolution. This conclusion implies the following: the tympanic membranes and the tympanic processes of the stapes in recent mammals, reptiles + birds. and frogs. are not homologous; the evolution of “special periotic systems” in the ancestors of amphibians and amniotes were independent events and preceded the evolution of tympanic membranes; the amphibian tympanic membrane. probably including that of labyrinthodonts. is not ancestral to that of amniotes. and that labyiinthodonts with an otic notch are not suitable as amniote ancestors; the stapes of early reptiles functioned primarily as part of the jaw suspension rather than in hearing; the mechanisms and abilities of sound perception in recent tetrapods are likely to be diverse rather than forming parts of a cline; and the lack of a tympanum in Gymnophiona and Caudata may be a retention of a primitive condition.     

The vertebrate middle and inner ear: A short overview

The evolution of the various hearing adaptations is connected to major structural changes in nearly all groups of vertebrates. Besides hearing, the detection of acceleration and orientation in space are key functions of this mechanosensory system. The symposium “show me your ear – the inner and middle ear in vertebrates” held at the 11th International Congress of Vertebrate Morphology (ICVM) 2016 in Washington, DC (USA) intended to present current research addressing adaptation and evolution of the vertebrate otic region, auditory ossicles, vestibular system, and hearing physiology. The symposium aimed at an audience with interest in hearing research focusing on morphological, functional, and comparative studies. The presented talks and posters lead to the contributions of this virtual issue highlighting recent advances in the vertebrate balance and hearing system. This article serves as an introduction to the virtual issue contributions and intends to give a short overview of research papers focusing on vertebrate labyrinth and middle ear related structures in past and recent years.     

The hyomandibulae of rhizodontids (Sarcopterygii, stem-tetrapoda)

Despite its important role in the study of the evolution of tetrapods, the hyomandibular bone (the homologue of the stapes in crown-group tetrapods) is known for only a few of the fish-like members of the tetrapod stem-group. The best-known example, that of the tristichopterid Eusthenopteron, has been used as an exemplar of fish-like stem-tetrapod hyomandibula morphology, but in truth the conditions at the base of the tetrapod radiation remain obscure. We report, here, four hyomandibulae, from three separate localities, which are referable to the Rhizodontida, the most basal clade of stem-tetrapods. These specimens share a number of characteristics, and are appreciably different from the small number of hyomandibulae reported for other fish-like stem-tetrapods. While it is unclear if these characteristics represent synapomorphies or symplesiomorphies, they highlight the morphological diversity of hyomandibulae within the early evolution of the tetrapod total-group. Well-preserved muscle scarring on some of these hyomandibulae permit more robust inferences of hyoid arch musculature in stem-tetrapods.     

The stapes of the Goal Measures embolomere Pholiderpeton scutigerum Huxley (Amphibia: Anthracosauria) and otic evolution in early tetrapods

Middle ear structure has been of interest for a long time in studies of the origins and relationships of early tetrapod groups. The model of a dorsally-directed, rod-like stapes with a tympanum, thought common to labyrinthodont amphibians, was taken to be primitive for tetrapods. The stapes of embolomeres and other early anthracosaurs were assumed to be of this form, but difficulties resulted if the middle ear structure of fossil and living reptiles was considered ultimately derived from this source.
The embolomere stapes has been identified and does not conform to the predicted model. It most closely resembles that of Greererpeton , an early notchless temnospondyl. The stapes is compared with those of other tetrapods in terms of the theoretical five processes. An interpretation is put forward in which all but the opercular are seen as potentially present. The embolomere stapes is compared with that of Greererpeton in terms of recent theories of mechanical function and is seen to weaken them. They are then compared as part of a possible acoustic mechanism. The embolomere middle ear structure is reinterpreted as a receiver for low-frequency sound and the 'otic notch' is not considered to have housed a tympanum.
The resemblance between the stapes of these two animals seems best explained by their closeness to the plesiomorphic condition for tetrapods, a conclusion which forces the abandonment of the concept of a 'labyrinthodont middle ear'. The middle ear structure of later groups can be interpreted as having evolved from one similar to that seen in these two animals. The conclusion supports those reached in other recent papers that tympana were not primitive for tetrapods but have been independently derived in several groups.     

On the use of osteoderm features in a phylogenetic approach on the internal relationships of the Chroniosuchia (Tetrapoda: Reptiliomorpha)

Abstract: Chroniosuchians are an enigmatic Permian to Triassic group of crocodile‐like basal tetrapods. Their conspicuous dorsal osteoderm systems include most of the group’s yet documented postcranial morphological variability but have hardly been considered in cladistic approaches. Aiming at the clarification of the internal relationships of the Chroniosuchia, we have carried out a parsimony analysis including, among others, 23 morphological and osteohistological osteoderm characters and 12 chroniosuchian taxa. According to the most parsimonious trees, taxa usually referred to Chroniosuchidae form a paraphyletic succession with Madygenerpeton pustulatus and Chroniosaurus dongusensis as the basalmost chroniosuchians and Uralerpeton tverdochlebovae as the sister group of Bystrowianidae (hypothesis A). However, the concurrent hypothesis of a basal split into monophyletic subtaxa Chroniosuchidae and Bystrowianidae (hypothesis B) is only slightly less parsimonious and supported by an alternative analysis which includes embolomeres as the only reptiliomorph outgroup. Searching for the better hypothesis, we compare the respective order of branching to the order of first occurrences in the fossil record, demonstrating that hypothesis A provides a better stratigraphic fit than hypothesis B. Accordingly, the last common ancestor of the yet known chroniosuchians had a series of broad complexly interlocking ‘chroniosuchid’ osteoderms that served as a protection carapace apart from supporting the trunk during terrestrial locomotion. The later evolution of chroniosuchian carapaces was marked by a stepwise increase in flexibility and size reduction, which resulted in a loss of protective function and in a reduction in trunk support function. The flexibility increase is paralleled by the evolution of the Crocodylomorpha whose extant members do not possess as extensively interlocking osteoderm systems as some of their Mesozoic relatives.     

The Smallest Known Tetrapod Footprints: Batrachichnus Salamandroides from the Carboniferous of Joggins,Nova Scotia,Canada

A new specimen of Batrachichnus salamandroides from the classic Carboniferous section at Joggins, Nova Scotia, is the smallest set of tetrapod footprints known in the fossil record. The trackmaker was a juvenile, quadrupedal temnospondyl or microsaur with a trunk length of 3.55 mm and an estimated body length of 8 mm (skull, presacral vertebrae, and caudal vertebrae). The 48 mm-long trackway preserves a high degree of extramorphological variation along its course, including a gait change associated with a change in direction along with an increased stride and pace, and the appearance of overstepped imprints, in the latter portion of the trackway. These morphological changes suggest the tetrapod changed from a walking gait to a running gait.     

Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear

The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (～160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non‐mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is “rod‐like” and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non‐mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher‐level phylogenetic hypotheses of mammals, the one we preferred places “haramiyidans” within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed “haramiyidans” outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between “haramiyidans” and other mammals. J. Morphol. 279:441–457, 2018. © 2016 Wiley Periodicals, Inc.     

The braincase of Typhlops and Leptotyphlops (Reptilia: Serpentes)

The structure of the braincases and associated nerves and blood-vessels is described. Typhlops combines primitive lacertilian features, notably the retention of a palatine artery, with specialisations such as the structure of the recessus scalae tympani. Leptotyphlops is more completely snake-like, but the two genera show in common a specialised intracranial course of the hyomandibular branch of the facial nerve, due to lateral closure of the juxtastapedial recess by the overgrowing crista circumfenestralis. The lateral closure of the juxtastapedial recess is considered as an adaptation to burrowing habits. The Vidian canal in scolecophidians is poorly defined, due to the lack of lateral ascending wings of the parasphenoid. This might constitute an archaic character contradicting the descent of snakes from any Recent lacertilian group.     

Homoplasy in the ear region of Tethytheria and the systematic position of Embrithopoda (Mammalia,Afrotheria)

The ear region of mammals has long been considered as morphologically very conservative and accordingly, phylogenetically useful. In this study, the anatomy of the petrosal and bony labyrinth (osseous inner ear) of Numidotherium (Proboscidea) and Arsinoitherium (Embrithopoda) are investigated and compared in order to assess the evolution of ear region characters in proboscideans and embrithopods. Using a cladistic analysis across Paenungulata based on ear region characters only, we found that Arsinoitherium is surprisingly best placed as a crown proboscideans to the exclusion of Numidotherium and Phosphatherium, which results in the paraphyly of proboscidean. The clade Proboscidea is actually well supported by dental and post-cranial characters, and we propose that this result underlines the great amount of morphological convergences in the ear region of Embrithopoda and Proboscidea, possibly due to convergent evolution of capabilities toward infrasonic hearing.     

The otic region of Doleserpeton (Temnospondyli) and its implications for the evolutionary origin of frogs

There is increasing evidence that the Palaeozoic temnospondyl amphibians had a frog‐like tympanic hearing system. For this reason, the otic region of Doleserpeton is described and compared with modern anurans. The otic capsules are expanded laterally and ventrally relative to other temnospondyls. The opisthotic has a bulbous ventral region resembling the ventrolateral ledge in modern frogs. Two lateral processes are located on the paroccipital process. Comparison with the condition in modern anurans with a tympanic hearing system shows that this may have been the attachment site for the tympanic annulus. Parts of the osseous labyrinth are also described. The inner ear shows numerous features resembling the condition found in frogs. These include strong evidence for the presence of a lissamphibian‐type perilymphatic duct most closely resembling that of anurans. This is the first time such a perilymphatic system has been described in any Palaezoic form. The posterior part of the braincase shows a jugular foramen closely associated with the perilymphatic foramen, as in anurans. Although the distribution of these traits among other temnospondyl groups remains little known, the sum of the evidence points to affinities between anurans and temnospondyls, and adds to the evidence for a close relationship between anurans and the Permian amphibamid Doleserpeton. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 738–751.     

The cranial morphology of Greererpeton burkemorani Romer (Amphibia: Temnospondyli)

The skull of Greererpeton burkemorani Romer, a temnospondyl amphibian from the Upper Mississippian at Greer, West Virginia is described. A detailed account of the stapes of a Mississippian amphibian is given for the first time and its function is discussed. It is suggested that the stapes formed the principal element of support for the back of the braincase and resisted potential dislocation of the otico-occipital region from the skull roof during contraction of the hypaxial musculature.
Greererpeton is included in the Colosteidae and an amended diagnosis of the family is given. Erpetosaurus differs from Colosteus, Greererpeton and Pholidogaster in the pattern of bones in the skull roof and palate, the dentition and the otic region and, consequently, it is removed from the Colosteidae. The Temnospondyli are considered to be a monophyletic group characterized by the development of a connection between the dorsal portion of the occipital arch, the exoccipital bones, and the skull roof. The loxommatids are removed from the Temnospondyli as they retain the plesiomorphic condition of braincase attachment which relies exclusively on derivatives of the auditory capsules.
On the basis of similarities in the structure of the braincase, palate and manus it is suggested that microsaurs are the collateral descendants (sister group) of temnospondyls. This relationship may account for the large number of similarities in the three living groups of Amphibia: Anura are generally believed to have descended from temnospondyls, while the Urodela and Apoda are often considered to have descended from microsaurs. These systematic conclusions endorse the recent suggestions that neither the Lepospondyli nor the Labyrinthodontia are natural groups, and both terms should be abandoned.     

The anatomy of the middle ear of the tinamiformes (Aves: Tinamidae)

The morphology of the middle ear region including the basicranium and quadrate of tinamous is compared among ratites and flying birds belonging to the Procellariiformes, Sphenisciformes, Pelecaniformes, and Ciconiiforms. The middle ears of tinamous and ratites share a number of important characters including absence of a separate foramen for the glossopharyngeal nerve; eustachian tube, carotid artery, and stapedial artery encased in bone; and a metotic process with vascular canals or notches. Outgroup analysis confirms these characters as synapomorphies. These data support the position that the Tinami and Ratiti form a monophyletic assemblage.     

The directionality of the ear of the pigeon (Columba livia)

Summary The directionality of cochlear microphonic potentials in the azimuthal plane was investigated in the pigeon (Columba livia), using acoustic free-field stimulation (pure tones of 0.25–6 kHz).At high frequencies in the pigeon's hearing range (4–6 kHz), changing azimuth resulted in a maximum change of the cochlear microphonic amplitude by about 20 dB (SPL). The directionality decreased clearly with decreasing frequency.Acoustic blocking of the contralateral ear canal could reduce the directional sensitivity of the ipsilateral ear by maximally 8 dB. This indicates a significant sound transmission through the bird's interaural pathways. However, the magnitude of these effects compared to those obtained by sound diffraction (maximum > 15 dB) suggests that pressure gradients at the tympanic membrane are only of subordinate importance for the generation of directional cues.The comparison of interaural intensity differences with previous behavioral results confirms the hypothesis that interaural intensity difference is the primary directional cue of azimuthal sound localization in the high-frequency range (2–6 kHz).Abbreviations CM cochlear microphonic potential - IID interaural intensity difference - IID-MRA minimum resolvable angle calculated from interaural intensity difference - MRA minimum resolvable angle - OTD interaural ongoing time difference - RMS root mean square - SPL sound pressure level     

The hyomandibular of Eusthenopteron foordi Whiteaves (Pisces: Crossopterygii) and the early evolution of the tetrapod stapes

The hyomandibular of Eusthenopteron foordi Whiteaves is briefly described and an attempt is made to reconcile discrepancies between previous accounts. The course of the branches of the truncus hyoideo-mandibularis (facial nerve VII) is discussed. The early evolution of the tetrapod stapes is considered in connection with the uncoupling of the head from the trunk and subsequent reduction in size ot the semicircular canals. The principal morphological character which distinguishes the stapes from the hyomandibular is found to be related to the course of the orbital (stapedial) artery and the truncus hyoideo-mandibularis.     

The cranial anatomy,ontogeny, and relationships of Karpinskiosaurus secundus (Amalitzky) (Seymouriamorpha,Karpinskiosauridae) from the Upper Permian of European Russia

The Upper Permian seymouriamorph tetrapod Karpinskiosaurus from European Russia includes two species: Karpinskiosaurus secundus and Karpinskiosaurus ultimus. Karpinskiosaurus secundus is represented by two specimens with skull lengths of about 75 mm. All specimens of K. ultimus are smaller than those of K. secundus. Revision of the cranial anatomy of all previously known and several new specimens of Karpinskiosaurus shows that the specimens of K. secundus and most of the specimens of K. ultimus represent the ontogenetic series of one species: K. secundus. The holotype specimen of K. ultimus requires revision, with the aim to find out whether it represents a second species of Karpinskiosaurus or not. The available material permits new reconstructions of the largest, holotype skull, and one smaller skull with a length of about 36 mm. Karpinskiosaurus secundus is included in a cladistic analysis for the first time here. The analysis shows it to form a sister taxon to Discosauriscidae. The clade comprising Karpinskiosaurus secundus plus Discosauriscidae forms a sister group to Seymouriidae. Karpinskiosaurus secundus has a large postorbital and a short preorbital region, and the orbits are placed in the posterior portion of the anterior half of the skull length. Among all seymouriamorphs, such cranial proportions are exhibited only by the largest known specimens of Discosauriscus austriacus. None of the specimens of K. secundus described here exhibits the presence of sensory grooves; thus, all specimens composing the ontogenetic sequence of K. secundus are considered to be terrestrial. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010.     

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology,development, and vision in the inner ear

Lungless salamanders (Family Plethodontidae) form a highly speciose group that has undergone spectacular adaptive radiation to colonize a multitude of habitats. Substantial morphological variation in the otic region coupled with great ecological diversity within this clade make plethodontids an excellent model for exploring the ecomorphology of the amphibian ear. We examined the influence of habitat, development, and vision on inner ear morphology in 52 plethodontid species. We collected traditional and 3D geometric morphometric measurements to characterize variation in size and shape of the otic endocast and peripheral structures of the salamander ear. Phylogenetic comparative analyses demonstrate structural convergence in the inner ear across ecologically similar species. Species that dwell in spatially complex microhabitats exhibit robust, highly curved semicircular canals suggesting enhanced vestibular sense, whereas species with reduced visual systems demonstrate reduced canal curvature indicative of relaxed selection on the vestibulo‐ocular reflex. Cave specialists show parallel enlargement of auditory‐associated structures. The morphological correlates of ecology among diverse species reveal underlying evidence of habitat specialization in the inner ear and suggest that there exists physiological variation in the function of the salamander ear even in the apparent absence of selective pressures on the auditory system to support acoustic behavior.