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Early development and orientation of the acoustic funnel provides insight into the evolution of sound reception pathways in cetaceans.

Yamato M, Pyenson ND - PLoS ONE (2015)

Bottom Line: In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation.In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway.Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

View Article: PubMed Central - PubMed

Affiliation: Departments of Vertebrate Zoology and Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, United States of America; Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, United States of America.

ABSTRACT
Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

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CT-based three-dimensional reconstructions of a toothed whale and baleen whale, right lateral view.Top: Stenella attenuata (USNM 504048). Bottom: Balaenoptera acutorostrata, juvenile specimen not part of this study. The tympanoperiotic complex houses the middle and inner ear structures, and is highlighted in yellow. The insert images are photographs of prepared tympanoperiotic complexes from mature individuals: B. bonarensis (USNM 504955) and S. attenuata (USNM 487880). The tympanic aperture is indicated by the blue arrow and the acoustic funnel is illustrated by the pink cone. Scale bar = 2 cm.
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pone.0118582.g001: CT-based three-dimensional reconstructions of a toothed whale and baleen whale, right lateral view.Top: Stenella attenuata (USNM 504048). Bottom: Balaenoptera acutorostrata, juvenile specimen not part of this study. The tympanoperiotic complex houses the middle and inner ear structures, and is highlighted in yellow. The insert images are photographs of prepared tympanoperiotic complexes from mature individuals: B. bonarensis (USNM 504955) and S. attenuata (USNM 487880). The tympanic aperture is indicated by the blue arrow and the acoustic funnel is illustrated by the pink cone. Scale bar = 2 cm.

Mentions: The acoustic funnel is separated from the tympanic aperture and the vestigial ear canal by the sigmoid process of the tympanic bone; therefore, the location of sound input for odontocetes is displaced anteriorly relative to the position of the tympanic aperture (Fig. 1). While sound reception mechanisms remain unclear in mysticetes, which do not have hollow mandibles filled with acoustic fats, there is new anatomical evidence suggesting that at least rorquals (Balaenopteridae) may also hear through fatty tissues associated with the ears [13]. These fatty tissues insert into the tympanoperiotic complex in an area that is homologous to the attachment site of odontocete acoustic fats, just anterior to the tympanic aperture and sigmoid process (Fig. 1; refer to [14–15] and S1 Text for anatomical terminology).


Early development and orientation of the acoustic funnel provides insight into the evolution of sound reception pathways in cetaceans.

Yamato M, Pyenson ND - PLoS ONE (2015)

CT-based three-dimensional reconstructions of a toothed whale and baleen whale, right lateral view.Top: Stenella attenuata (USNM 504048). Bottom: Balaenoptera acutorostrata, juvenile specimen not part of this study. The tympanoperiotic complex houses the middle and inner ear structures, and is highlighted in yellow. The insert images are photographs of prepared tympanoperiotic complexes from mature individuals: B. bonarensis (USNM 504955) and S. attenuata (USNM 487880). The tympanic aperture is indicated by the blue arrow and the acoustic funnel is illustrated by the pink cone. Scale bar = 2 cm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4356564&req=5

pone.0118582.g001: CT-based three-dimensional reconstructions of a toothed whale and baleen whale, right lateral view.Top: Stenella attenuata (USNM 504048). Bottom: Balaenoptera acutorostrata, juvenile specimen not part of this study. The tympanoperiotic complex houses the middle and inner ear structures, and is highlighted in yellow. The insert images are photographs of prepared tympanoperiotic complexes from mature individuals: B. bonarensis (USNM 504955) and S. attenuata (USNM 487880). The tympanic aperture is indicated by the blue arrow and the acoustic funnel is illustrated by the pink cone. Scale bar = 2 cm.
Mentions: The acoustic funnel is separated from the tympanic aperture and the vestigial ear canal by the sigmoid process of the tympanic bone; therefore, the location of sound input for odontocetes is displaced anteriorly relative to the position of the tympanic aperture (Fig. 1). While sound reception mechanisms remain unclear in mysticetes, which do not have hollow mandibles filled with acoustic fats, there is new anatomical evidence suggesting that at least rorquals (Balaenopteridae) may also hear through fatty tissues associated with the ears [13]. These fatty tissues insert into the tympanoperiotic complex in an area that is homologous to the attachment site of odontocete acoustic fats, just anterior to the tympanic aperture and sigmoid process (Fig. 1; refer to [14–15] and S1 Text for anatomical terminology).

Bottom Line: In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation.In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway.Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

View Article: PubMed Central - PubMed

Affiliation: Departments of Vertebrate Zoology and Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, United States of America; Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, United States of America.

ABSTRACT
Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

Show MeSH
Related in: MedlinePlus