Better than fish on land? Hearing across metamorphosis in salamanders

Christensen, Christian Bech; Lauridsen, Henrik; Christensen‐Dalsgaard, Jakob; Pedersen, Marianne Bruus; Madsen, Peter T.

doi:10.1098/rspb.2014.1943

Cited by 37 publications

(24 citation statements)

References 53 publications

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“…They may therefore be hypothesized to be unable to detect aerial sound pressure. However, vibration sensitivity has been shown to enable atympanic vertebrates such as snakes and likely also salamanders to sense airborne sound through detection of sound-induced head vibrations (Christensen et al, 2012;Christensen et al, 2015). It is therefore possible that lungfish are also able to sense airborne sound via a similar mechanism.…”

Section: Introductionmentioning

confidence: 99%

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Christensen

Christensen‐Dalsgaard

Madsen

2015

Journal of Experimental Biology

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In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-toparticle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods.

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Section: Introductionmentioning

confidence: 99%

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Christensen

Christensen‐Dalsgaard

Madsen

2015

Journal of Experimental Biology

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“…Christensen et al state ( [1], p. 2), 'Equally important, [the urodele auditory system] can be regarded as a potential model for the intermediate evolutionary developmental stage' between lungfish and frogs. However, there is strong evidence that salamanders have secondarily lost a tympanic ear, which dramatically changes the interpretation of the results of this study.…”

Section: Salamanders Are Not Evolutionary Intermediatesmentioning

confidence: 99%

“…Christensen et al [1] assert that microsaurs are morphological exemplars for the early tetrapod condition (a rationale for this was not provided) and that similarities of the middle ear can be used to associate the functional data derived from salamanders with the early evolution of frog-like hearing. This is problematic for two reasons.…”

Section: Microsaurs Are Not Representative Of Early Tetrapodsmentioning

confidence: 99%

“…

Christensen et al recently published a study of hearing in neotenic and experimentally metamorphosed axolotls (Ambystoma mexicanum) and a larval and adult tiger salamander (A. tigrinum), which contributes greatly to our understanding of salamander sound perception in water and air [1]. They demonstrate that premetamorphic, atympanic aquatic salamanders are capable of perceiving high frequency airborne sounds similar to terrestrial adults, demonstrating an interesting capacity for an atympanic ear to function for sound perception in a variety of media.

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confidence: 99%

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Is there an exemplar taxon for modelling the evolution of early tetrapod hearing?

et al. 2016

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Christensen et al. recently published a study of hearing in neotenic and experimentally metamorphosed axolotls (Ambystoma mexicanum) and a larval and adult tiger salamander (A. tigrinum), which contributes greatly to our understanding of salamander sound perception in water and air [1]. They demonstrate that premetamorphic, atympanic aquatic salamanders are capable of perceiving high frequency airborne sounds similar to terrestrial adults, demonstrating an interesting capacity for an atympanic ear to function for sound perception in a variety of media. This important research, in combination with other recent studies on the sound perception capabilities of lungfish [2], is helping to better clarify issues related to the water-to-land transition. However, the implication of their experimental design demands a consideration of the evolutionary history of their selected exemplar taxa so these valuable data can be interpreted in a broader context. Our criticisms focus on two major points: the use of salamanders as a proxy for hearing ability intermediate between aquatic and terrestrial vertebrates, and the use of microsaurs as exemplars of the early tetrapod condition.The currently accepted hypothesis for the origin of a tympanic ear is as a derivation from the spiracle of sarcopterygian fish [3]. In 'fish' the spiracle is associated with gill breathing: water passes through the spiracular notch in the rear of the skull, past the braincase and the bracing hyomandibula, to the oropharynx and gill arches [4]. With the loss of gills, the persisting spiracular lumen is co-opted into a middle ear chamber, and the cranial support role of the hyomandibula (now termed stapes) is eliminated, leaving this bone to extend freely into the middle ear chamber (figure 1). In derived tetrapods, the spiracular opening is expanded and covered by a membrane (the tympanum) that collects sound. Vibrations are transmitted to the inner ear via the stapes, which becomes more delicate and better able to propagate fine vibrations [7][8][9][10].

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“…

We thank Anderson et al [1] for engaging in our paper on hearing in salamanders [2]. We have written our paper primarily as experimental physiologists basing hypotheses on recent animals and with no research expertise in palaeontology.

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confidence: 99%

In defence of comparative physiology: ideal models for early tetrapods do not exist

Christensen

Lauridsen

Christensen‐Dalsgaard

et al. 2016

Proc. R. Soc. B.

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We thank Anderson et al. [1] for engaging in our paper on hearing in salamanders [2]. We have written our paper primarily as experimental physiologists basing hypotheses on recent animals and with no research expertise in palaeontology. Therefore, discussions with palaeontologists are especially welcome. In many ways, palaeontology should constrain our hypotheses and the finding of a fossil tympanate urodele, for example, could change our views, as could more information on the ear region of the early tetrapods. It is also true that comparative physiology has erred in its ways previously-by comparing disparate living exemplar species and inferring that such a lineup reflects evolutionary history (i.e. naming recent species as 'lower', 'primitive' or 'ancestral'). A stellar example is the older view of the tympanate ear originating in the tetrapod ancestors with the recent groups-anurans, lizards, archosaurs and mammals exemplifying different stages in the evolution of the middle ear. This view has been abandoned, based on the thorough palaeontological investigations by Clack [3,4] and others showing independent origins of the tympanate ear in all the major groups.When this is said, we find the criticism to be misdirected concerning two major points, the first being the use of model animals. Anderson et al. state that 'Salamanders are not evolutionary intermediates' and with that we fully agree; we certainly do not regard salamanders or any other living creatures as evolutionary intermediates, 'missing links' or even as 'exemplar species'. Furthermore, to designate any living species as 'exemplar' seems to us to revert to the practices described above-any living species will only be superficially similar to the ancient species and may, in the best case, illustrate some aspects of its physiology. Rather, the solid comparative approach would be to investigate many recent species (i.e. to compare the physiology of salamanders, caecilians and earless frogs and infer ancestral physiology from common features). Another strategy in comparative physiology is to use living organisms to investigate biological solutions to problems common to fossils and (unrelated) recent animals-for example, to use large mammals as models for large dinosaurs. Anderson et al. claim that salamanders are an inappropriate model, because 'there is strong evidence that salamanders have secondarily lost a tympanic ear' and this 'dramatically changes the interpretation of the results of' our study [2]. Now, it is probable that salamanders are secondarily reduced, also in their middle ear configuration, but it is by no means certain that their ancestors were tympanate. This is most likely under the temnospondyl hypothesis; under the lepospondyl hypothesis, the divergence-dating by Pyron [5] suggests a caudate -anuran split at 292 Ma, long before the atympanate proanuran Triadobatrachus, and so making a tympanate ancestry of salamanders much less likely. However, even if the salamanders are secondarily reduced from tympanate ancestors they could sti...

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Better than fish on land? Hearing across metamorphosis in salamanders

Cited by 37 publications

References 53 publications

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Is there an exemplar taxon for modelling the evolution of early tetrapod hearing?

In defence of comparative physiology: ideal models for early tetrapods do not exist

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