Head morphology in perinatal dolphins: A window into phylogeny and ontogeny

Rauschmann, Michael; Huggenberger, Stefan; Kossatz, Lars S.; Oelschläger, Helmut

doi:10.1002/jmor.10477

Cited by 45 publications

(55 citation statements)

References 91 publications

(181 reference statements)

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“…Consequently, we conclude that directional asymmetry in archaeocetes is related to hearing. This finding is consistent with odontocete ontogeny: at perinatal stages, spotted dolphins (Stenella attenuata) exhibit incipient cranial and facial asymmetry, whereas the mandibular fat body and pan bone are already fully developed (31). Cranial asymmetry reaches an adult degree soon after birth in the harbor porpoise Phocoena phocoena (6).…”

Section: Discussionsupporting

confidence: 79%

Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water

Fahlke¹,

Gingerich²,

Welsh

et al. 2011

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

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Eocene archaeocete whales gave rise to all modern toothed and baleen whales (Odontoceti and Mysticeti) during or near the Eocene-Oligocene transition. Odontocetes have asymmetrical skulls, with asymmetry linked to high-frequency sound production and echolocation. Mysticetes are generally assumed to have symmetrical skulls and lack high-frequency hearing. Here we show that protocetid and basilosaurid archaeocete skulls are distinctly and directionally asymmetrical. Archaeocete asymmetry involves curvature and axial torsion of the cranium, but no telescoping. Cranial asymmetry evolved in Eocene archaeocetes as part of a complex of traits linked to directional hearing (such as pan-bone thinning of the lower jaws, mandibular fat pads, and isolation of the ear region), probably enabling them to hear the higher sonic frequencies of sound-producing fish on which they preyed. Ultrasonic echolocation evolved in Oligocene odontocetes, enabling them to find silent prey. Asymmetry and much of the sonic-frequency range of directional hearing were lost in Oligocene mysticetes during the shift to lowfrequency hearing and bulk-straining predation.Cetacea | land-to-sea transition M ost mammals have bilaterally symmetrical skulls. Symmetrical crania characterize the artiodactyls closely related to whales, and symmetrical crania characterize mysticetes within Cetacea (1) (Fig. 1A). Odontocetes are exceptional because most odontocete crania are asymmetrical, with dorsal cranial bones shifted posteriorly and to the left side (1-8). Living odontocetes have a hypertrophied melon, nasal sacs, and phonic lips used to produce high-frequency sound (> 20 kHz) (9-11). Mysticetes lack these specializations of the nasal apparatus, use low-frequency sound (11,12), and may use the larynx (13) to produce lowfrequency sound. Coupling of high-frequency echolocation with facial and cranial asymmetry in living odontocetes, and the absence of both in living artiodactyls and living mysticetes, make it reasonable to expect that asymmetry originated in odontocetes (5-7). However, it is unresolved how the cranial asymmetry of odontocetes evolved in the transition from archaeocetes to modern whales, and the history becomes even more complex when archaeocetes themselves are considered.Eocene archaeocete whales gave rise to all modern toothed and baleen whales during or near the Eocene-Oligocene transition (14-16). Archaeocetes were previously thought to have symmetrical skulls (3, 5, 7). Asymmetry observed in fossil crania has often been assumed to be an artifact of deformation following burial, and it has been ignored or even removed in published drawings [as was done initially for three of the skulls we studied (17-19)]. ResultsHere we document and quantify asymmetry in archaeocete crania. Further observations on exceptionally well-preserved archaeocete crania and dentaries suggest a link between cranial asymmetry and the ability to locate sound sources in water.We quantified midline suture deviation, δx, from a straight rostrocaudal axis [RC, after Ness...

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Section: Discussionsupporting

confidence: 79%

Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water

Fahlke¹,

Gingerich²,

Welsh

et al. 2011

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

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“…Accordingly, the musculature in the epicranial complex of the sperm whale is likely homologous to that of dolphins innervated by the facial nerve (Mead, 1975;Rauschmann, 1992;Rommel et al, 2002Rommel et al, , 2009Rauschmann et al, 2006;Huggenberger et al, 2009). In contrast to the situation in non-cetacean mammals, this cranial nerve runs without significant ramification from the tympanoperiotic complex to and below the orbita, turns upward around the lateral margin of the skull roof via the antorbital notch, and then ramifies strongly in order to innervate the blowhole musculature (Rauschmann, 1992;Rommel et al, 2002Rommel et al, , 2009).…”

Section: Homologies In Toothed Whale Forehead Structuresmentioning

confidence: 99%

The nose of the sperm whale: overviews of functional design, structural homologies and evolution

2014

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The hypertrophic and much elongated epicranial (nasal) complex of sperm whales (Physeter macrocephalus) is a unique device to increase directionality and source levels of echolocation clicks in aquatic environments. The size and shape of the nasal fat bodies as well as the peculiar organization of the air sac system in the nasal sound generator of sperm whales are in favour of this proposed specialized acoustic function. The morphology of the sperm whale nose, including a 'connecting acoustic window' in the case and an anterior 'terminal acoustic window' at the rostroventral edge of the junk, supports the 'bent horn hypothesis' of sound emission. In contrast to the laryngeal mechanism described for dolphins and porpoises, sperm whales may drive the initial pulse generation process with air pressurized by nasal muscles associated with the right nasal passage (right nasal passage muscle, maxillonasolabialis muscle). This can be interpreted as an adaptation to deep-diving and high hydrostatic pressures constraining pneumatic phonation. Comparison of nasal structures in sperm whales and other toothed whales reveals that the existing air sac system as well as the fat bodies and the musculature have the same topographical relations and thus may be homologous in all toothed whales (Odontoceti). This implies that the nasal sound generating system evolved only once during toothed whale evolution and, more specifically, that the unique hypertrophied nasal complex was a main driving force in the evolution of the sperm whale taxon.

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“…All these structures are involved in the pneumatic generation of echolocation (ultrasound) and communication (sound) signals. Thus the facial nerve runs as a strong trunk along the side of the head from the stylomastoid foramen via the zygomatic arch, and through the antorbital notch in the skull roof to the blowhole musculature [Huggenberger, 2004;Rauschmann et al, 2006;Comtesse-Weidner, 2007;Oelschläger et al, 2008;Huggenberger et al, 2009;Mead and Fordyce, 2009;Huggenberger and Oelschläger, in press]. Baleen whales, in contrast, do not exhibit such a highly specialized epicranial complex and might produce sounds in the larynx or laryngeal sacs.…”

Section: Functional Aspects Of Brainstem Structuresmentioning

confidence: 99%

Cetacean Brain Evolution: Dwarf Sperm Whale <i>(Kogia sima)</i> and Common Dolphin <i>(Delphinus delphis)</i> – An Investigation with High-Resolution 3D MRI

2010

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This study compares a whole brain of the dwarf sperm whale (Kogia sima) with that of a common dolphin (Delphinus delphis) using high-resolution magnetic resonance imaging (MRI). The Kogia brain was scanned with a Siemens Trio Magnetic Resonance scanner in the three main planes. As in the common dolphin and other marine odontocetes, the brain of the dwarf sperm whale is large, with the telencephalic hemispheres remarkably dominating the brain stem. The neocortex is voluminous and the cortical grey matter thin but expansive and densely convoluted. The corpus callosum is thin and the anterior commissure hard to detect whereas the posterior commissure is well-developed. There is consistency as to the lack of telencephalic structures (olfactory bulb and peduncle, olfactory ventricular recess) and neither an occipital lobe of the telencephalic hemisphere nor the posterior horn of the lateral ventricle are present. A pineal organ could not be detected in Kogia. Both species show a tiny hippocampus and thin fornix and the mammillary body is very small whereas other structures of the limbic system are well-developed. The brain stem is thick and underlies a large cerebellum, both of which, however, are smaller in Kogia. The vestibular system is markedly reduced with the exception of the lateral (Deiters’) nucleus. The visual system, although well-developed in both species, is exceeded by the impressive absolute and relative size of the auditory system. The brainstem and cerebellum comprise a series of structures (elliptic nucleus, medial accessory inferior olive, paraflocculus and posterior interpositus nucleus) showing characteristic odontocete dimensions and size correlations. All these structures seem to serve the auditory system with respect to echolocation, communication, and navigation.

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Head morphology in perinatal dolphins: A window into phylogeny and ontogeny

Cited by 45 publications

References 91 publications

Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water

Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water

The nose of the sperm whale: overviews of functional design, structural homologies and evolution

Cetacean Brain Evolution: Dwarf Sperm Whale <i>(Kogia sima)</i> and Common Dolphin <i>(Delphinus delphis)</i> – An Investigation with High-Resolution 3D MRI

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