Patterns and processes in the early evolution of the tetrapod ear

This article reviews some of the latest information on the evolution of the tetrapod ear region as seen in the fossil record. It looks at the changes that can be documented across the fish-tetrapod transition, the patterns that they show and what can be inferred of the processes that brought some of them about. These processes include an increased role for neural crest, and heterochronic processes such as pedomorphosis. The earliest tetrapods show a common pattern of a short stout stapes with a large stapedial foramen, that primitively contacted the palatal bones and probably supported the braincase. Modifications to this pattern can be seen in tandem with changes to the occiput and are bound up with changes to jaw and breathing mechanisms. By the Late Carboniferous, tetrapods had diversified into a range of groups showing a wide variety of otic morphologies, some of which were probably tympanic, while others were not, and some which are very different from those found in extant tetrapods. In amniotes, the evolution of a tympanic ear appears to correlate with consolidation and integration of the occiput to the skull roof. Competing phylogenies suggest different numbers of iterations for the origin of a tympanic ear, but a minimum of four separate occasions is implied.     

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.     

Some introductory notes on the organization of the forebrain in tetrapods.

As an introduction to the main theme of this conference an overview of the organization of the tetrapod forebrain is presented with emphasis on the telencephalic representation of sensory and motor functions. In all classes of tetrapods, olfactory, visual, octavolateral, somatosensory and gustatory information reaches the telencephalon. Major differences exist in the telencephalic targets of sensory information between amphibians and amniotes. In amphibians, three targets are found: the lateral pallium for olfactory input, the medial pallium for visual and multisensory input, and the lateral subpallium for visual, octavolateral and somatosensory information. The forebrains of reptiles and mammals are similar in that the dorsal surface of their cerebral hemisphere is formed by a pallium with three major segments: (a) an olfactory, lateral cortex; (b) a 'limbic' cortex that forms the dorsomedial wall of the hemisphere, and (c) an intermediate cortex that is composed entirely of isocortex in mammals, but in reptiles (and birds) consists of at least part of the dorsal cortex (in birds the Wulst) and a large intraventricular protrusion, i.e. the dorsal ventricular ridge. In birds, the entire lateral wall of the hemisphere is involved in this expansion. The intermediate pallial segment receives sensory projections from the thalamus and contains modality-specific sensory areas in reptiles, birds and mammals. The most important differences between the intermediate pallial segment of amniotes concern motor systems.     

Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping

Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages.     

The Evolution of the Tetrapod Middle Ear in the Rhipidistian-Amphibian Transition

From a survey ot the structure of the skull in rhipidistianfishes and early labylinthodont Amphibia and of the mechanismof hearing in these two groups, an account of the evolutionof the tetrapod middle ear is presented. The overall modificationof the otic region of the skull during the rhipidistian-amphibiantransition is analyzed in terms of changes in different organsystems in response to different selective pressures (affecting,for example, the feeding, respiratory, and locomotory mechanisms).These changes are seen to occur in a completely integrated pattern.Considerations of the different requirements for sound receptionunder water and in air, in connection with this correlated progressionof evolutionary change in the otic region of the head, revealthe manner in which the hyomandibular, spiracular diverticulum,and operculum of rhipidistian fishes became modified to formthe stapes, the tympanic cavity, and the outer portion of thetympanum, respectively, of tetrapods.     

Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?

Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.     

The amphibian octavo-lateralis system and its regressive and progressive evolution

The phylogenetic and ontogenetic changes in the octavolateralis system of sarcopterygian fish and tetrapods, presumed to be important for the formation of an amphibian auditory system, are reviewed. The lateral line system shows rudimentation of lines and loss of ampullary electroreceptors in many amphibians; in some amphibians it never develops. The metamorphic changes of the lateral-line system show different patterns in the different amphibian lineages with metamorphic retention in most urodeles and metamorphic loss in most anurans. The multitude of both ontogenetic and phylogenetic changes of the lateral line system among amphibians do exclude any prediction as to how this system might have changed in ancestral amniotes. The most important auditory epithelium of the tetrapod inner ear, the basilar papilla, seems to be primitively present in all tetrapods and Latimeria. In two amphibian lineages there is a trend towards rudimentation and loss of the basilar papilla. Only in the third order, the anurans, a tympanic ear develops and the inner ear shows a progressive evolution of the auditory epithelia. Together with the known differences in the periotic labyrinth of amphibians and amniotes, this scenario suggests a parallel evolution of the amniotic and anuran auditory periphery. All mechanoreceptive hair cells of the lateral line system and the inner ear appear to receive a common and bilateral efferent innervation. Among amphibians this pattern is represented only in some urodeles, whereas anurans show a derived pattern with loss of a bilateral component and presumably also of a common neuromast/inner ear component. Changes in the rhombencephalic nuclei which receive octavo-lateralis afferent fibers show a trend towards development of auditory nuclei only in the anuran lineage. The phylogenetic appearance of an auditory nucleus in this lineage coincides with the complete absence of formation of ampullary electroreceptors. In contrast, the earlier claim of a correlation between a metamorphic loss of the lateral line system and the formation of an auditory nucleus is not supported by more recent data: an auditory nucleus develops in anurans already prior to metamorphosis and is present in all anurans even when they retain the neuromast system. In anurans with a metamorphic loss of the neuromasts, the second order neurons degenerate as well. This independence of the auditory and the second order lateral line nuclei is further substantiated by their separate projection to other brain areas, like the torus semicircularis of the midbrain, and their functional properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

Arthropod remains in the oral cavities of fossil reptiles support inference of early insectivory

Inference of feeding preferences in fossil terrestrial vertebrates (tetrapods) has been drawn predominantly from craniodental morphology, and less so from fossil specimens preserving conclusive evidence of diet in the form of oral and/or gut contents. Recently, the pivotal role of insectivory in tetrapod evolution was emphasized by the identification of putative insectivores as the closest relatives of the oldest known herbivorous amniotes. We provide the first compelling evidence for insectivory among early tetrapods on the basis of two 280-million-year-old (late Palaeozoic) fossil specimens of a new species of acleistorhinid parareptile with preserved arthropod cuticle on their toothed palates. Their dental morphology, consisting of homodont marginal dentition with cutting edges and slightly recurved tips, is consistent with an insectivorous diet. The intimate association of arthropod cuticle with the oral region of two small reptiles, from a rich fossil locality that has otherwise not produced invertebrate remains, strongly supports the inference of insectivory in the reptiles. These fossils lend additional support to the hypothesis that the origins and earliest stages of higher vertebrate evolution are associated with relatively small terrestrial insectivores.     

MICROSAURS AND THE ORIGIN OF CAPTORHINOMORPH REPTILES

Microsaurs are Paleozoic lepospondylous Amphibia with slenderbodies and weak limbs. Their solidly roofed skulls lack oticnotches, have large supratemporals widely separating the squamosalfrom parietal, and double occipital condyles. The stapes consistsof a large footplate and extremely short columella. Vertebraelack intercentra. Originally based on a reptile, Hylonomus lyelli,by Dawson in 1863, the Order Microsauria has long been restrictedto these small amphibians (Romer, 1950). Repeated confusionbetween primitive captorhinomorph reptiles and microsaurs steinsfrom superficial similarities between both skulls and vertebrae.This confusion and occasional microsaur-like vertebrae in earlyCarboniferous deposits have led to suggestions that microsaursare reptilian ancestors (cf. Vaughn, 1962). Captorhinomorphs differ from microsaurs in their small supratemporalbone, single occipital condyle, stapes with long columella reachinga pit in the quadrate and bearing a dorsal process, and dorsalintercentra. Captorhinomorph ancestors were probably not labyrinthodonts,as Vaughn (1960) has pointed out, but they could not have hadthe characteristic specializations of microsaurs. Their sourcemust be sought in forms much closer to crossopterygian fish. Microsaurs resemble both urodeles and gymnophionans in theirdouble occipital joint and otic region. They differ from Lissamphibiain the absence of a non-calcified zone in the teeth. At present,no criteria indicate decisively which structures developed convergently.Microsaurs are possibly but not demonstrably related to theancestry of modern salamanders and caecilians.     

Pterygoideus muscles and other jaw adductors in amphibians and reptiles

The general structural patterns of jaw adductors in all orders of extant amphibians and reptiles, and also polypteriforms, crossopterygians (coelacanth), and dipnoans, are compared. The pterygoideus muscles probably developed independently and in parallel in gymnophions and amniotes from the profound pseudotemporalis muscle, which was present in their fishlike ancestors and was retained in caudate and anuran amphibians. The functional causes of the development of pterygoideus muscles in the majority of tetrapod groups and the absence of these muscles in Urodela and Anura are discussed. The anterior pterygoideus muscle of crocodiles is homologous to the pseudotemporalis (superficial) muscle of other reptiles.     

Ecological succession among late palaeozoic and mesozoic tetrapods

Natural selection and the development of new taxa are associated with ecological replacement and the increase in number of niches with time. Continental faunal interchange was possible globally because of the existence of the super-continent Pangaea during much of the Upper Palaeozoic and Mesozoic. Figures of tetrapod niches vs. time and discussion of this concept for that period are presented for the first time. Four habitat divisions are used, namely marine, fresh-water, lowland and upland.The marine habitat was colonised rather late by tetrapods and these may have been the first predators on the early bony fishes which had diversified in the Permian. The radiation of bony fishes in the Jurassic was followed by a further increase in variety of their reptilian predators. Predators seem to develop some time after the radiation of a new potential prey group.Most early amphibians occupied fresh-water habitats in “crocodile” or “frog” niches, but from the Triassic tetrapods moved from fresh-waters and lowlands into the uplands also.In terrestrial habitats, the replacement of mammal-like reptiles by dinosaurs is tentatively explained in terms of palaeoclimatology and thermoregulatory physiology. Ornithischians capable of dealing with tough vegetation evolved to occupy the new niches produced by the radiation of conifers in the Jurassic. The extinction of dinosaurs appears to have been connected with temperature and habitat changes.Conclusions are supported by a summary of published opinions on the palaeoecological roles of early tetrapods.     

Why is limb regeneration possible in amphibians but not in reptiles,birds, and mammals?

The capacity to regenerate limbs is very high in amphibians and practically absent in other tetrapods despite the similarities in developmental pathways and ultimate morphology of tetrapod limbs. We propose that limb regeneration is only possible when the limb develops as a semiautonomous module and is not involved in interactions with transient structures. This hypothesis is based on the following two assumptions: To an important extent, limb development uses the same developmental mechanisms as normal limb development and developmental mechanisms that require interactions with transient structures cannot be recapitulated later. In amniotes limb development is early, shortly after neurulation, and requires inductive interactions with transient structures such as somites. In amphibians limb development is delayed relative to amniotes and has become decoupled from interactions with somites and other transient structures that are no longer present at this stage. The limb develops as a semi-independent module. A comparison of the autonomy and timing of limb development in different vertebrate taxa supports our hypothesis and its assumptions. The data suggest a good correlation between self-organizing and regenerative capacity. Furthermore, they suggest that whatever barriers amphibians overcame in the evolution of metamorphosis, they are the same barriers that need to be overcome to make limb regeneration possible in other taxa.     

Phylogeny of the major tetrapod groups: Morphological data and divergence dates

Summary The phylogeny of the major groups of tetrapods (amphibians, reptiles, birds, and mammals) has until recently been poorly understood. Cladistic analyses of morphological data are producing new hypotheses concerning the relationships of the major groups, with a focus on the identification of monophyletic groups. Molecular phylogenies support some of these views and dispute others. Geological dates of the major evolutionary branching points are recalculated on the basis of the cladograms and new fossil finds.     

Links between global taxonomic diversity,ecological diversity and the expansion of vertebrates on land

Tetrapod biodiversity today is great; over the past 400 Myr since vertebrates moved onto land, global tetrapod diversity has risen exponentially, punctuated by losses during major extinctions. There are links between the total global diversity of tetrapods and the diversity of their ecological roles, yet no one fully understands the interplay of these two aspects of biodiversity and a numerical analysis of this relationship has not so far been undertaken. Here we show that the global taxonomic and ecological diversity of tetrapods are closely linked. Throughout geological time, patterns of global diversity of tetrapod families show 97 per cent correlation with ecological modes. Global taxonomic and ecological diversity of this group correlates closely with the dominant classes of tetrapods (amphibians in the Palaeozoic, reptiles in the Mesozoic, birds and mammals in the Cenozoic). These groups have driven ecological diversity by expansion and contraction of occupied ecospace, rather than by direct competition within existing ecospace and each group has used ecospace at a greater rate than their predecessors.     

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 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.     

Homologies in the fossil record: The middle ear as a test case

This paper examines the middle ear of fossil living animals in terms of the homologies which have been drawn between its parts in different vertebrate groups. Seven homologies are considered: 1, the middle ear cavity/spiracular pouch; 2, the stapes/hyomandibula; 3, the stapedial/hyomandibular processes; 4 the tympanic membrane; 5, the otic notch; 6, the fenestra ovalis; 7, and the stapedial/hyomandibular foramen. The reasons leading to assessments of homology are reviewed. Homologies 1 and 2, based largely on embryological evidence, are fairly robust, though there are arguments about the details. Homologies 3, 4 and 5 stem from ideas about early tetrapod evolution, and were influenced by contingent factors including the order and time of discovery of early fossil taxa, and perceptions of their phylogeny which resulted from this. They were also influenced by ideas of the evolution of terrestriality among tetrapods. Most of the conceptions have been overturned in recent years by new fossil discoveries and new ways of looking at old data. Homology 6 has been little considered. One possible hypothesis, placed in a strictly archetypal theoretical framework has been ignored but deserves consideration on other grounds. Homology 7 depends on how tetrapods are characterised, not a question which has posed difficulties until recently, but which is likely to with the discovery of intermediate fossil forms.     

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.     

Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis

The dermal bone sculpture of early, basal tetrapods of the Permo-Carboniferous is unlike the bone surface of any living vertebrate, and its function has long been obscure. Drawing from physiological studies of extant tetrapods, where dermal bone or other calcified tissues aid in regulating acid-base balance relating to hypercapnia (excess blood carbon dioxide) and/or lactate acidosis, we propose a similar function for these sculptured dermal bones in early tetrapods. Unlike the condition in modern reptiles, which experience hypercapnia when submerged in water, these animals would have experienced hypercapnia on land, owing to likely inefficient means of eliminating carbon dioxide. The different patterns of dermal bone sculpture in these tetrapods largely correlates with levels of terrestriality: sculpture is reduced or lost in stem amniotes that likely had the more efficient lung ventilation mode of costal aspiration, and in small-sized stem amphibians that would have been able to use the skin for gas exchange.