Evolution of the amphibian tympanic ear and the origin of frogs

Recent anurans plus all but the most primitive temnospondyl labyrinthodont amphibians are proposed as a monophyletic taxon, based on shared stapedial characters which are derived with respect to all other tetrapods. Within temnospondyls, the mostly Lower Permian dissorophoids are proposed as most closely related to Recent anurans, based on interpretation of the dissorophoid dorsal quadrate process and the anuran tympanic annulus as sequential steps in a character transformation series. The otic features described here reinforce the concept of the amphibian tympanic ear as a prior "invention" with no genealogical relationship to amniote tympanic ears.     

The stapes of Edops craigi and ear evolution in the lissamphibian stem group

The Lower Permian temnospondyl Edops craigi exemplifies an early and plesiomorphic condition of the single ear ossicle or stapes among the temnospondyls, the probable stem group of lissamphibians. In Edops, the 11-cm-long bone is more massive than in other temnospondyls, has a distinct neck, a dorsal crest and incompletely subdivided footplate and ventral process. Despite a range of invariances, temnospondyl stapes were much more diverse than previously conceived. A survey of described stapes gives insight into character evolution of the ear ossicle in the lissamphibian stem group. These include alternative patterns of paedomorphosis, proportional size change, morphology of tympanic region and reorientation of the auditory apparatus.     

The braincase and middle ear region of Dendrerpeton acadianum (Tetrapoda: Temnospondyli)

Dendrerpeton acadianum from the Westphalian A (Upper Carboniferous) of Joggins, Nova Scotia, is a phylogenetically and chronologically early temnospondyl. Its external cranial anatomy has been used previously to suggest the presence of a tympanic membrane, and thus of an ear adapted to the perception of airborne sound. However, supporting evidence provided by stapedial and braincase morphology has so far been lacking. The braincase and middle ear region have remained almost wholly unknown. CT scanning and 3-D computer reconstruction of BMNH R.436 have been used to shed light on these important areas. Both stapes prove to be present in the specimen; the right stapes is distorted, but the left stapes lies inside the cranial cavity and is perfectly preserved. The latter resembles the stapes of the relatively few other temnospondyls in which the bone has been described and is most similar to that of Doleserpeton . The morphology and orientation of the stapes provide strong evidence for the presence of an ear adapted to the perception of airborne sound, with similarities to the extant anuran condition. The reconstructed braincase shows a high degree of similarity to that of other adequately known temnospondyls. This gives supporting evidence that D. acadianum is correctly placed in the temnospondyl phylogeny and thus demonstrates one of the earliest hearing systems adapted to the perception of airborne sound that can be homologized with the extant anuran condition.  © 2005 The Trustees of the Natural History Museum, Zoological Journal of the Linnean Society , 2005, 143 , 577−597.     

The origin of modern amphibians: a re‐evaluation

There are currently three competing hypotheses seeking to explain the evolutionary origins of modern amphibians. The lepospondyl hypothesis holds that the lysorophian lepospondyls constitute the sister taxon to all lissamphibians. The temnospondyl hypothesis suggests that modern amphibians are most closely related to the dissorophoid temnospondyls. Finally, the polyphyletic hypothesis posits that the modern amphibian orders have separate evolutionary origins from among different groups of Palaeozoic tetrapods. Here, we review the character matrices used in previous studies. These data sets differ significantly in choice of characters. Therefore, we built a matrix based on data from all three hypotheses and analysed key taxa phylogenetically using both Bayesian inference and parsimony. Uncorrected, the supermatrix yielded inconclusive results, demonstrating the presence of at least two phylogenetic optima. When the data were corrected according to new observations on Doleserpeton, Eocaecilia, and other fossil forms, the phylogeny supported the temnospondyl hypothesis of lissamphibian origins. This conclusion is also supported by a careful study of character changes in the individual lineages. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 457–469.     

Braincase evolution in suchian archosaurs (Reptilia: Diapsida): evidence from the rauisuchian Batrachotomus kupferzellensis

The osteology of an almost complete braincase of the rauisuchian archosaur Batrachotomus kupferzellensis Gower from the Middle Triassic of Germany is described. There is a possibly discrete epiotic ossification, the metotic fissure is undivided by bone (i.e. there is a metotic foramen), the medial wall of the otic capsule is mostly ossified, the cerebral branch of the internal carotid artery entered the lateral surface of the parabasisphenoid, the ventral ramus of the opisthotic is more prominent laterally than a strong subvertical ridge on the exoccipital and basioccipital that lies posterior to the external foramen for the hypoglossal nerve, and the perilymphatic foramen faces away from the otic capsule in a posterior direction. Braincase morphology in the rauisuchians Saurosuchus galilei , Postosuchus kirkpatricki, and Tikisuchus romeri is reviewed. A matrix of 27 braincase characters for 12 archosaurian taxa is analysed. The most parsimonious hypothesis is consistent with the currently orthodox view of archosaurian phylogeny, except in that aetosaurians are more closely related to crocodylomorphs than is any rauisuchian. This phylogeny is used in a brief interpretation of the evolution of derived braincase features present in extant crocodilians. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 136 , 49–76.     

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.     

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.     

Amphibian Body Impressions from the Mississippian of Pennsylvania,USA

Temnocorpichnus isaacleai is a new ichnogenus and ichnospecies of temnospondyl amphibian body impression from the Mississippian (Visean) Mauch Chunk Formation of eastern Pennsylvania, United States. The shovel-shaped head, robust limbs, relatively short trunk and smooth integument diagnose the ichnotaxon and readily distinguish it from Hermundurichnus and Sauropleura, the only other named body impressions of Paleozoic tetrapods. Temnocorpichnus is a compound ichnogenus in which the footprint ichnogenus Batrachichnus is a behaviorally distinct component. The temnospondyl identity of Temnocorpichnus adds to the sparse and earliest records of temnspondyls, which are of Visean age. The smooth integument of the ichnogenus does not support the presence of ventral scales or armor in the earliest temnospondyls, but body proportions of the Mauch Chunk body impressions indicate a relatively terrestrial temnospondyl not matched by any taxon now known from bones. Three closely associated impressions of Temnocorpichnus on a single bedding plane suggest some sort of gregarious behavior in Mississippian temnospondyls and may support speculation that internal fertilization and associated courtship behavior evolved independently in one group of amphibians more than 300 million years ago.     

AMPHIBIANS FROM THE MIDDLE JURASSIC BALABANSAI SVITA IN THE FERGANA DEPRESSION, KYRGYZSTAN (CENTRAL ASIA)

Abstract: Larval and metamorphosed Ferganobatrachus riabinini (Temnospondyli, Brachyopoidea), metamorphosed Kokartus honorarius (Caudata, Karauridae), an indeterminated karaurid (Karauridae indet.) and, presumably, anurans (?Anura indet.) are represented by isolated cranial and postcranial skeletal elements in the Middle Jurassic (Bathonian–Callovian) Balabansai Svita of the Fergana Depression, Kyrgyzstan. The Balabansai vertebrate assemblage is one of the few faunas in which non‐lissamphibian temnospondyls, stem caudates and anurans occur together. The presence of a supraglenoid foramen and a complex strap‐like glenoid on the scapulocoracoid in Kokartus supports its basal phylogenetic position within the Caudata.     

First direct evidence of a vertebrate three-level trophic chain in the fossil record

We describe the first known occurrence of a Permian shark specimen preserving two temnospondyl amphibians in its digestive tract as well as the remains of an acanthodian fish, which was ingested by one of the temnospondyls. This exceptional find provides for the first time direct evidence of a vertebrate three-level food chain in the fossil record with the simultaneous preservation of three trophic levels. Our analysis shows that small-sized Lower Permian xenacanthid sharks of the genus Triodus preyed on larval piscivorous amphibians. The recorded trophic interaction can be explained by the adaptation of certain xenacanthids to fully freshwater environments and the fact that in these same environments, large temnospondyls occupied the niche of modern crocodiles. This unique faunal association has not been documented after the Permian and Triassic. Therefore, this Palaeozoic three-level food chain provides strong and independent support for changes in aquatic trophic chain structures through time.     

The evolution of the scalation pattern in temnospondyl amphibians

In most Palaeozoic temnospondyls, thin round-oval scales covering the flanks and the back of the trunk can be distinguished from ventral, elongate gastral scales arranged in a chevron pattern. The extensive growth series of the temnospondyl Sclerocephalus reveals that the morphology of the gastral scales in small larvae corresponds to the round-oval scales of the rest of the body. During subsequent ontogeny, the gastral scales differentiate and attain a spindle-shaped morphology. The tapering end of each gastral scale fits into a dorsal groove on the medial adjacent scale. This arrangement allowed telescoping of the scales and thus provided a high degree of flexibility. In the ontogenetically most advanced specimens of Sclerocephalus the gastral scales attain a rhomboid outline, and the articulation by well-defined facets has reduced the flexibility between them. In most temnospondyls, the gastral scales retain the 'juvenile' spindle-shape or the 'larval' round-oval shape, which can be interpreted as a paedomorphic trait. This suggests that the different types of gastral scales in temnospondyls, as well as the scales of the back and the flanks, can be traced back to the same Anlage of round-oval scales that differentiated early in ontogeny. In the Mesozoic, a complete reduction of dermal scalation occurred independently in distinct dissorophoid, capitosauroid, and trematosauroid temnospondyls. This reduction was probably the result of several factors unique to each group, such as cutaneous respiration, the demand for greater mobility, and the decreased importance of belly protection in fully aquatic temnospondyls.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 150 , 815–834.     

Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics

In this study we recorded auditory brainstem responses to airborne sounds to determine the hearing sensitivity of Xenopus laevis frogs and correlated their hearing profiles with middle ear characteristics. In newly metamorphosed frogs (body mass 0.5–0.76 gm, snout-vent length 17–20 mm) best hearing sensitivities were measured in the 2.4–2.8 kHz range, whereas optimal hearing sensitivity of older adults (body mass 18–90 gm; snout-vent length 57–100 mm) ranged from 1.0 to 1.2 kHz. Middle ear volumes reconstructed from serial sections showed approximate volume of 0.002 cc and 0.04–0.07 cc in newly metamorphosed and older frogs, respectively. This inverse frequency–volume relationship is consistent with the properties of an acoustic resonator indicating that differences in best hearing sensitivity are at least in part correlated to variation in middle ear volumes for airborne sounds. These results are consistent with peak frequency vibrational velocity profiles of Xenopus tympanic disk that have been shown to be dependent on underlying middle ear volumes and corroborate the occurrence of peak amplitudes of otoacoustic emissions in the 1.0–1.2 kHz region in adult Xenopus frogs.     

The skull and jaw musculature as guides to the ancestry of salamanders

The fossil record provides no evidence supporting a unique common ancestry for frogs, salamanders and apodans. The ancestors of the modern orders may have diverged from one another as recently as 250 million years ago, or as long ago as 400 million years according to current theories of various authors. In order to evaluate the evolutionary patterns of the modern orders it is necessary to determine whether their last common ancestor was a rhipidistian fish, a very primitive amphibian, a labyrimhodom or a ‘lissamphibian’. The broad cranial similarities of frogs and salamanders, especially the dominance of the braincase as a supporting element, can be associated with the small size of the skull in their immediate ancestors. Hynobiids show the most primitive cranial pattern known among the living salamander families and “provide a model for determining the nature of the ancestors of the entire order. Features expected in ancestral salamanders include: (1) Emargination of the cheek; (2) Movable suspensorium formed by the quadrate, squamosal and pterygoid; (3) Occipital condyle posterior to jaw articulation; (4) Distinct prootic and opisthotic; (5) Absence ol otic notch; (6) Stapes forming a structural link between braincase and cheek. In the otic region, cheek and jaw suspension, the primitive salamander pattern (resembles most closely the microsaurs among known Paleozoic amphibians, and shows no significant features in common with either ancestral frogs or the majority of labyrinth odonts. The basic pattern of the adductor jaw musculature is consistent within both frogs and salamanders, but major differences are evident between the two groups. The dominance of the adductor mandibulae externus in salamanders can be associated with the open cheek in all members of that order, and the small size of this muscle in frogs can be associated with the large otic notch. The spread of different muscles over the otic capsule, the longus head ol the adductor mandibulae posterior in frogs and the superficial head of the adductor mandibulae internus in salamanders, indicates that fenestration of the skull posterodorsal to the orbit occurred separately in the ancestors of the two groups. Reconstruction of the probable pattern of the jaw musculature in Paleozoic amphibians indicates that frogs and salamanders might have evolved from a condition hypothesized for primitive labyrinthodonts, but the presence of a large otic notch in dissorophids suggests specialization toward the anuran, not the urodele condition. The presence of either an einarginated cheek or an embayment of the lateral surface of the dentary and the absence of an otic notch in microsaurs indicate a salamander-like distribution of die adductor jaw muscles. The ancestors of frogs and salamanders probably diverged from one another in the early Carboniferous, Frogs later evolved from small labyrinthodonts and salamanders from microsaurs. Features considered typical of lissamphibians evolved separately in the two groups in the late Permian andTriassic.     

New data on the braincase of the aetosaurian archosaur (Reptilia: Diapsida) Stagonolepis robertsoni Agassiz

New data on the braincase of the aetosaurian archosaur Stagonolepis robertsoni Agassiz are presented, based on new preparation, synthetic casting, and interpretation of fossil material from the Triassic Elgin Sandstones, Scotland. The metotic fissure is not divided by bone. The perilymphatic foramen is completely bound by bone, and faces away from the otic capsule in a posterolateral direction. A prominent subvertical ridge on the anterolateral edge of the exoccipital and upper part of the basioccipital cannot be directly associated with the subcapsular process of the chondrocranium of extant crocodilians. This ridge projects laterally beyond the ventral ramus of the opisthotic, and lies anterior to the external foramina for the hypoglossal nerve. The overall structure of the braincases (especially the otic region) of S. robertsoni and other aetosaurians, where known, is more similar (in terms of derived archosaurian characters) to those of crocodylomorphs than are the braincases of other major suchian groups. This provides evidence for the currently unorthodox hypothesis that, among major suchian clades, Aetosauria and Crocodylomorpha are each others' closest relatives. Support for this hypothesis is found in features of the palatine and prefrontal that have not been considered in recent studies of suchian phylogeny. This alternative phylogenetic hypothesis demands further investigation but, combined with the new morphological data that it explains, it provides a framework for the understanding of the evolution of the derived and distinctive braincase structure of extant crocodilians.  © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society, 2002, 136 , 7−23.     

An invasive species imposes selection on life‐history traits of a native frog

As well as their direct ecological impacts on native taxa, invasive species can impose selection on phenotypic attributes (morphology, physiology, behaviour, etc.) of the native fauna. In anurans, body size at metamorphosis is a critical life‐history trait: for most challenges faced by post‐metamorphic anurans, larger size at metamorphosis probably enhances survival. However, our studies on Australian frogs (Limnodynastes convexiusculus) show that this pattern can be reversed by the arrival of an invasive species. When metamorph frogs first encounter invasive cane toads (Bufo marinus), they try to eat the toxic invader and, if they are able to do so, are likely to die from poisoning. Because frogs are gape‐limited predators, small metamorphs cannot ingest a toad and thus survive long enough to disperse away from the natal pond (and thus from potentially deadly toads). These data show that larger size at metamorphosis can reduce rather than increase anuran survival rates, because larger metamorphs are more easily able to ingest (and thus be poisoned by) metamorph cane toads. Our results suggest that patterns of selection on life‐history traits of native taxa (such as size and age at metamorphosis, seasonal timing of breeding and duration of pondside aggregation prior to dispersal) can be modified by the arrival of an invasive species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 329–336.     

Patterns of praying mantis auditory system evolution based on morphological, molecular, neurophysiological, and behavioural data

Some praying mantids have sensitive ultrasonic hearing arising from a unique 'cyclopean' ear located in the ventral metathorax. The present study explores the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioural, and molecular databases. Using an 'auditory phylogeny' based on 13 morphological characters, we identified a primitively earless form of metathoracic anatomy in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Superimposing these results onto a phylogenetic tree derived from molecular data from seven genes shows that the cyclopean mantis ear evolved once approximately 120 Mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multicomponent, in-flight behaviour triggered by ultrasound. Thus, mantids have an ancient, highly conserved auditory neural–behavioural system. Although ultrasonic hearing in several insect groups evolved in response to bat predation, mantis hearing predates the appearance of bats (approximately 63 Mya) and must originally have functioned in communication, prey detection, or avoidance of nonbat predators.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 541–568.     

Revisiting the contribution of larval characters to an analysis of phylogenetic relationships of basal anurans

The higher-level relationships of anurans have been explored by numerous studies, producing a variety of hypotheses. The relationships of the basal anurans ('archaeobatrachians') are, however, poorly known . In part, this may be because the adult morphology of basal anurans is derived and therefore may not provide suitable phylogenetic signal. Recently, several authors have shown the phylogenetic utility of information derived from anuran larvae. In this paper we conduct separate and combined analyses of anuran relationships based on adult and larval morphology. Our combined results suggest that anurans form two major clades − the pipoids and all other frogs. Evidence also suggests that, taken together, Neobatrachia and Pelobatoidea form a monophyletic group. We discuss support for various groupings as shown by the different data sets. We also comment on the consequences of our phylogenetic hypothesis for the interpretation of reduction of vertebral elements and evolution of Orton's tadpole types in anurans.  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society, 2003, 139 , 129−155.