Dataset Information

Low-frequency hearing preceded the evolution of giant body size and filter feeding in baleen whales.

ABSTRACT: Living baleen whales (mysticetes) produce and hear the lowest-frequency (infrasonic) sounds among mammals. There is currently debate over whether the ancestor of crown cetaceans (Neoceti) was able to detect low frequencies. However, the lack of information on the most archaic fossil mysticetes has prevented us from determining the earliest evolution of their extreme acoustic biology. Here, we report the first anatomical analyses and frequency range estimation of the inner ear in Oligocene (34-23 Ma) fossils of archaic toothed mysticetes from Australia and the USA. The cochlear anatomy of these small fossil mysticetes resembles basilosaurid archaeocetes, but is also similar to that of today's baleen whales, indicating that even the earliest mysticetes detected low-frequency sounds, and lacked ultrasonic hearing and echolocation. This suggests that, in contrast to recent research, the plesiomorphic hearing condition for Neoceti was low frequency, which was retained by toothed mysticetes, and the high-frequency hearing of odontocetes is derived. Therefore, the low-frequency hearing of baleen whales has remained relatively unchanged over the last approximately 34 Myr, being present before the evolution of other signature mysticete traits, including filter feeding, baleen and giant body size.

SUBMITTER: Park T

PROVIDER: S-EPMC5310610 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Low-frequency hearing preceded the evolution of giant body size and filter feeding in baleen whales.

Park Travis T Evans Alistair R AR Gallagher Stephen J SJ Fitzgerald Erich M G EM

Proceedings. Biological sciences 20170201 1848

Living baleen whales (mysticetes) produce and hear the lowest-frequency (infrasonic) sounds among mammals. There is currently debate over whether the ancestor of crown cetaceans (Neoceti) was able to detect low frequencies. However, the lack of information on the most archaic fossil mysticetes has prevented us from determining the earliest evolution of their extreme acoustic biology. Here, we report the first anatomical analyses and frequency range estimation of the inner ear in Oligocene (34-23 ...[more]

PMID: 28179519

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Project description:Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum VO2 at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half VO2|max. These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations.

Project description:Background:Family Cetotheriidae sensu stricto and several closely related taxa comprise the Cetotherioidea and represent a lineage of Neogene baleen whales that includes the smallest edentulous baleen whales in Earth history. Most of known cetotheriids came from the Late Miocene to Quaternary, and the earliest records from the latest Middle Miocene. The Paratethys region shows a great diversity of Middle to Late Miocene cetotheriids. That includes nominative taxon of the family, Cetotherium rathkii, and this suggests that the earliest cetotheriids may have lived in that region. Materials and methods:Here, Ciuciulea davidi, a new genus and species from the Middle Miocene of southeastern Europe, is described as the chronologically earliest and earliest diverging member of Cetotheriidae. Also, a new specimen of Otradnocetus, a basal Cetotherioidea sensu Gol'din & Steeman, 2015 is identified from the Late Miocene deposits of Caucasus and compared with Otradnocetus virodovi from the Middle Miocene of the same region. Results and discussion:Ciuciulea davidi is a dwarf whale displaying primitive traits: posterior ends of facial bones forming a single transverse line, a narrow occipital shield, and a relatively long interparietal region. Meanwhile, it shares some cetotheriid apomorphies: posteriorly telescoped wedge-shaped facial bones and an ovoid tympanic bulla with shallow lateral and medial furrows, a short anterior lobe and a short sigmoid process. Phylogenetic analysis suggests that Parietobalaena and Otradnocetus are branches diverging before the clade Cetotheriidae + Neobalaenidae. This is confirmed by the stepwise evolution of the anatomy of the squamosal, mandible, and ear bones across these groups. The re-described juvenile specimen of Otradnocetus differs from O. virodovi in the more primitive anatomy of the mandible and the autapomorphic anatomy of the humerus. Records of the earliest cetotheriids and related taxa in the Paratethys support the idea that this could be the region where Cetotheriidae evolved before their worldwide dispersal and radiation.

Dataset Information

Low-frequency hearing preceded the evolution of giant body size and filter feeding in baleen whales.

Publications

Low-frequency hearing preceded the evolution of giant body size and filter feeding in baleen whales.

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