Fossil evidence on evolution of inner ear cochlea in Jurassic mammals

Luo, Zhe‐Xi; Ruf, Irina; Schultz, Julia A.; Martin, Thomas

doi:10.1098/rspb.2010.1148

Cited by 87 publications

(95 citation statements)

References 31 publications

(66 reference statements)

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“…Remaining quiet during the day, A. musicus perhaps managed not to raise the attention of contemporary diurnal Archaeopteryx-like reptiles. We cannot rule out the possibility that Jurassic mammals (e.g., Morganucodon and Dryolestes) might have been predators of these insects, as they were able to hear sounds in the range of frequencies used by A. musicus (31,32).…”

Section: Discussionmentioning

confidence: 99%

Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females

Montealegre‐Z²,

Robert³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Behaviors are challenging to reconstruct for extinct species, particularly the nature and origins of acoustic communication. Here we unravel the song of Archaboilus musicus Gu, Engel and Ren sp. nov., a 165 million year old stridulating katydid. From the exceptionally preserved morphology of its stridulatory apparatus in the forewings and phylogenetic comparison with extant species, we reveal that A. musicus radiated pure-tone (musical) songs using a resonant mechanism tuned at a frequency of 6.4 kHz. Contrary to previous scenarios, musical songs were an early innovation, preceding the broad-bandwidth songs of extant katydids. Providing an accurate insight into paleoacoustic ecology, the low-frequency musical song of A. musicus was well-adapted to communication in the lightly cluttered environment of the mid-Jurassic forest produced by coniferous trees and giant ferns, suggesting that reptilian, amphibian, and mammalian insectivores could have also heard A. musicus' song.call evolution | Tettigoniidae | bushcricket | biomechanics | biological asymmetry K atydids produce species-specific calling songs that form part of the acoustic ecology of tropical forests (1, 2). The rubbing of a toothed vein on one wing against a plectrum on the other wing results in sound production by stridulation, exploiting resonant (musical) (3, 4) or nonresonant (broadband) (4, 5) biophysical mechanisms, depending on the species. Which of these two mechanisms represents ancestral sound production remains a key question in the evolution of insect acoustic communication (6)(7)(8). Here, we reconstruct the song of a katydid fossil with exceptionally well-preserved stridulatory structures, and find that musical singing at low frequencies was already established by the middle Jurassic (165 Ma). We describe this specimen as Archaboilus musicus, from the extinct family Haglidae (Orthoptera), a group basal to all extant katydids (9, 10). These findings imply that A. musicus was nocturnal, and that its call was adapted for long-range communication in an environment with light clutter (11). A recent paleobotanical reconstruction of the geometry, vegetation density, and biomass of the Jurassic Forest from northwest China (12) reveals an environment populated by coniferous trees (e.g., Araucaria) with nearest neighbor distances ranging from 1.5 to 20.3 m, and giant ferns (e.g., Angiopteris, Osmunda, and Caniopteris) occupying the lower layers of the understory forest. This forest architecture indicates a sparse vegetation density that is acoustically compatible with the proposition that the song frequency of A. musicus was well adapted to long-distance communication close to the ground. Such a forested environment would also enable long-range acoustic signaling and communication by other animals (e.g., amphibians, reptilians) as well as a variety of arthropod species (13). Systematic PaleontologyInsecta Linnaeus, 1758; Orthoptera Olivier, 1789; Haglidae Handlirsch, 1906; Cyrtophyllitinae Zeuner, 1935; Archaboilus Martynov, 1937.Archaboilus musicu...

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Section: Discussionmentioning

confidence: 99%

Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females

Montealegre‐Z²,

Robert³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…The primary and secondary osseous spiral laminae are visible in the cochlear canal, as in Notostylops (Macrini et al 2010) and therians generally (Meng & Fox, 1995;Luo et al 2011). The primary osseous spiral lamina projects from the meatal (inner) wall of the cochlear canal (e.g.…”

Section: Cochlear Canalmentioning

confidence: 99%

“…Cells of this ganglion synapse with cochlear hair cells (Gray, 1977;Luo & Marsh, 1996). The tractus spiralis foraminosus, which connects the spiral ganglion canal to cranial nerve VIII within the internal auditory meatus (Gray, 1977;Luo et al 2011), is visible on the CT images of Altitypotherium (Fig. 3d).…”

Section: Cochlear Canalmentioning

confidence: 99%

Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters

Macrini

Flynn

et al. 2013

Journal of Anatomy

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The phylogenetic relationships of notoungulates, an extinct group of predominantly South American herbivores, remain poorly resolved with respect to both other placental mammals and among one another. Most previous phylogenetic analyses of notoungulates have not included characters of the internal cranium, not least because few such features, including the bony labyrinth, have been described for members of the group. Here we describe the inner ears of the notoungulates Altitypotherium chucalensis (Mesotheriidae), Pachyrukhos moyani (Hegetotheriidae) and Cochilius sp. (Interatheriidae) based on reconstructions of bony labyrinths obtained from computed tomography imagery. Comparisons of the bony labyrinths of these taxa with the basally diverging notoungulate Notostylops murinus (Notostylopidae), an isolated petrosal from Itabora ı, Brazil, referred to Notoungulata, and six therian outgroups, yielded an inner ear character matrix of 25 potentially phylogenetically informative characters, 14 of them novel to this study. Two equivocally optimized character states potentially support a pairing of Mesotheriidae and Hegetotheriidae, whereas four others may be diagnostic of Notoungulata. Three additional characters are potentially informative for diagnosing more inclusive clades: one for crown Placentalia; another for a clade containing Kulbeckia, Zalambdalestes, and Placentalia; and a third for Eutheria (crown Placentalia plus stem taxa). Several other characters are apomorphic for at least one notoungulate in our study and are of potential interest for broader taxonomic sampling within Notoungulata to clarify currently enigmatic interrelationships. Measures of the semicircular canals were used to infer agility (e.g. capable of quick movements vs. lethargic movements) of these taxa. Agility scores calculated from these data generally corroborate interpretations based on postcranial remains of these or closely related species. We provide estimates of the lowfrequency hearing limits in notoungulates based on the ratio of radii of the apical and basal turns of the cochlea. These limits range from 15 Hz in Notostylops to 149 Hz in Pachyrukhos, values comparable to the Asian elephant (Elephas maximus) and the California sea lion (Zalophus californianus) when hearing in air, respectively.

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“…404 forms the largest part of the osseous labyrinth by volume (table 3). The canal is coiled in Huayqueriana, as is universally the case in therians (Luo et al, 2010); it expresses a total helical rotation of 795°, equivalent to 2.2 full turns ( fig. 21F; table 3).…”

Section: Osseous Inner Earmentioning

confidence: 99%

Exceptional Skull of Huayqueriana (Mammalia, Litopterna, Macraucheniidae) From the Late Miocene of Argentina: Anatomy, Systematics, and Paleobiological Implications

Forasiepi

MacPhee

Pino

et al. 2016

Bulletin of the American Museum of Natural History

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Fossil evidence on evolution of inner ear cochlea in Jurassic mammals

Cited by 87 publications

References 31 publications

Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females

Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females

Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters

Exceptional Skull of Huayqueriana (Mammalia, Litopterna, Macraucheniidae) From the Late Miocene of Argentina: Anatomy, Systematics, and Paleobiological Implications

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