Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids

Kitazawa, Takatoshi; Takechi, Masaki; Hirasawa, Tatsuya; Adachi, Noritaka; Narboux-Nême, Nicolas; Kume, Hideaki; Maeda, Kazuhiro; Hirai, Takamasa; Miyagawa‐Tomita, Sachiko; Kurihara, Yukiko; Hitomi, Jiro; Levi, Giovanni; Kuratani, Shigeru; Kurihara, Hiroki

doi:10.1038/ncomms7853

Cited by 63 publications

(69 citation statements)

References 44 publications

(52 reference statements)

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“…Comparisons of jaw development in mouse and chick support the paleontological findings. The relative positions of the primary jaw joint and the first pharyngeal pouch led to the coupling of tympanic membrane formation with the lower jaw in mammals and with the upper jaw in diapsids [Kitazawa et al, 2015]. In the mammalian ancestors, the primary jaw joint moved dorsally, eventually associating the lower jaw with the tympanum and tympanic ring (a structure derived from lower jaw elements).…”

Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

“…Mammalian middle ear bones were derived from the hyomandibular bone and from both upper and lower jaw elements. In diapsids, the hyomandibular decoupled from the quadrate to form the columella, or stapes, and the position of the primary jaw joint did not move [Kitazawa et al, 2015]. Thus tympanic hearing is a true evolutionary novelty that arose in parallel multiple times [Clack 1997; Christensen-Dalsgaard and Carr, 2008], most likely in the Triassic, 100 MY after the origin of tetrapods.…”

Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

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Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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The earliest vertebrate ears likely subserved a gravistatic function for orientation in the aquatic environment. However, in addition to detecting acceleration created by the animal's own movements, the otolithic end organs that detect linear acceleration would have responded to particle movement created by external sources. The potential to identify and localize these external sources may have been a major selection force in the evolution of the early vertebrate ear and in the processing of sound in the central nervous system. The intrinsic physiological polarization of sensory hair cells on the otolith organs confers sensitivity to the direction of stimulation, including the direction of particle motion at auditory frequencies. In extant fishes, afferents from otolithic end organs encode the axis of particle motion, which is conveyed to the dorsal regions of first-order octaval nuclei. This directional information is further enhanced by bilateral computations in the medulla and the auditory midbrain. We propose that similar direction-sensitive neurons were present in the early aquatic tetrapods and that selection for sound localization in air acted upon preexisting brain stem circuits like those in fishes. With movement onto land, the early tetrapods may have retained some sensitivity to particle motion, transduced by bone conduction, and later acquired new auditory papillae and tympanic hearing. Tympanic hearing arose in parallel within each of the major tetrapod lineages and would have led to increased sensitivity to a broader frequency range and to modification of the preexisting circuitry for sound source localization.

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Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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“…A pivotal new paper by Kitazawa et al [9] confirms the parallel evolution of eardrums in at least two tetrapod lineages by showing that the tympanum forms in different ways in mouse and chicken. Tracing the formation of the jaw showed that the lower-to-upper jaw transformation induced by inactivation of the Endothelin1-Dlx5/6 cascade involving Goosecoid results in loss of the tympanic membrane in mouse, but causes duplication of the tympanic membrane in chicken [9].…”

Section: Tympanic Hearing Is a True Evolutionary Noveltymentioning

confidence: 99%

“…Tracing the formation of the jaw showed that the lower-to-upper jaw transformation induced by inactivation of the Endothelin1-Dlx5/6 cascade involving Goosecoid results in loss of the tympanic membrane in mouse, but causes duplication of the tympanic membrane in chicken [9]. Different development of the jaw joint and first pharyngeal pouch, perhaps related to feeding or breathing strategies, could have led to the coupling of tympanic membrane formation to the lower jaw in mammals and to the upper jaw in birds (Figure 1).…”

Section: Tympanic Hearing Is a True Evolutionary Noveltymentioning

confidence: 99%

Evolutionary trends in directional hearing

Carr

Christensen‐Dalsgaard

2016

Current Opinion in Neurobiology

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Tympanic hearing is a true evolutionary novelty that arose in parallel within early tetrapods. We propose that in these tetrapods, selection for sound localization in air acted upon pre-existing directionally sensitive brainstem circuits, similar to those in fishes. Auditory circuits in birds and lizards resemble this ancestral, directionally sensitive framework. Despite this anatomically similarity, coding of sound source location differs between birds and lizards. In birds, brainstem circuits compute sound location from interaural cues. Lizards, however, have coupled ears, and do not need to compute source location in the brain. Thus their neural processing of sound direction differs, although all show mechanisms for enhancing sound source directionality. Comparisons with mammals reveal similarly complex interactions between coding strategies and evolutionary history.

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“…ing range [Manley, 2010], evolved independently in mammals and birds [Lombard and Bolt, 1979;Clack, 1997;Kitazawa et al, 2015]. It is thus currently assumed that the auditory hindbrain nuclei in these two tetrapod groups reflect independent evolution and therefore represent homoplasious structures, i.e.…”

mentioning

confidence: 99%

Comparative Analysis of Gene Regulatory Network Components in the Auditory Hindbrain of Mice and Chicken

Pawlik

Schlüter²,

Hartwich³

et al. 2016

Brain Behav Evol

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The neurons in the mammalian and avian auditory hindbrain nuclei share a number of significant morphological and physiological properties for fast, secure and precise neurotransmission, such as giant synapses, voltage-gated K⁺ channels and fast AMPA receptors. Based on the independent evolution of the middle ear in these two vertebrate lineages, on different embryonic origins of the nuclei and on marked differences on the circuit level, these similarities are assumed to reflect convergent evolution. Independent acquisition of similar phenotypes can be produced by divergent evolution of genetic mechanisms or by similar molecular mechanisms. The distinction between these two possibilities requires knowledge of the gene regulatory networks (GRNs) that orchestrate the development of auditory hindbrain structures. We therefore compared the expression pattern of GRN components, both transcription factors (TFs) and noncoding RNA, during terminal differentiation of the auditory hindbrain structures in mouse and chicken when neurons acquire their final morphological and electrophysiological properties. In general, we observed broad expression of these genes in the mouse auditory cochlear nucleus complex and the superior olivary complex at both postnatal day 4 (P4) and at P25, and for the chicken at the equivalent developmental stages, i.e. embryonic day 13 (E13) and at P14-P17. Our data are in agreement with a model based on similar molecular mechanisms underlying terminal differentiation and maintenance of neuronal cell identity in the auditory hindbrain of different vertebrate lineages. This conservation might reflect developmental constraints arising from the tagmatic organization of rhombomeres and the evolutionarily highly conserved GRNs operating in these structures.

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Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids

Cited by 63 publications

References 44 publications

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Evolutionary trends in directional hearing

Comparative Analysis of Gene Regulatory Network Components in the Auditory Hindbrain of Mice and Chicken

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