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      Ultrasonic hearing and echolocation in the earliest toothed whales

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      Biology Letters
      The Royal Society

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          Abstract

          <p class="first" id="d5935666e177">The evolution of biosonar (production of high-frequency sound and reception of its echo) was a key innovation of toothed whales and dolphins (Odontoceti) that facilitated phylogenetic diversification and rise to ecological predominance. Yet exactly when high-frequency hearing first evolved in odontocete history remains a fundamental question in cetacean biology. Here, we show that archaic odontocetes had a cochlea specialized for sensing high-frequency sound, as exemplified by an Oligocene xenorophid, one of the earliest diverging stem groups. This specialization is not as extreme as that seen in the crown clade. Paired with anatomical correlates for high-frequency signal production in Xenorophidae, this is strong evidence that the most archaic toothed whales possessed a functional biosonar system, and that this signature adaptation of odontocetes was acquired at or soon after their origin. </p>

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          Most cited references14

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          Radiation of Extant Cetaceans Driven by Restructuring of the Oceans

          The remarkable fossil record of whales and dolphins (Cetacea) has made them an exemplar of macroevolution. Although their overall adaptive transition from terrestrial to fully aquatic organisms is well known, this is not true for the radiation of modern whales. Here, we explore the diversification of extant cetaceans by constructing a robust molecular phylogeny that includes 87 of 89 extant species. The phylogeny and divergence times are derived from nuclear and mitochondrial markers, calibrated with fossils. We find that the toothed whales are monophyletic, suggesting that echolocation evolved only once early in that lineage some 36–34 Ma. The rorqual family (Balaenopteridae) is restored with the exclusion of the gray whale, suggesting that gulp feeding evolved 18–16 Ma. Delphinida, comprising all living dolphins and porpoises other than the Ganges/Indus dolphins, originated about 26 Ma; it contains the taxonomically rich delphinids, which began diversifying less than 11 Ma. We tested 2 hypothesized drivers of the extant cetacean radiation by assessing the tempo of lineage accumulation through time. We find no support for a rapid burst of speciation early in the history of extant whales, contrasting with expectations of an adaptive radiation model. However, we do find support for increased diversification rates during periods of pronounced physical restructuring of the oceans. The results imply that paleogeographic and paleoceanographic changes, such as closure of major seaways, have influenced the dynamics of radiation in extant cetaceans.
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            Functional morphology and homology in the odontocete nasal complex: implications for sound generation.

            The site and physiologic mechanism(s) responsible for the generation of odontocete biosonar signals have eluded investigators for decades. To address these issues we subjected postmortem toothed whale heads to interrogation using medical imaging techniques. Most of the 40 specimens (from 19 species) were examined using x-ray computed tomography (CT) and/or magnetic resonance imaging (MR). Interpretation of scan images was aided by subsequent dissection of the specimens or, in one case, by cryosectioning. In all specimens we described a similar tissue complex and identified it as the hypothetical biosonar signal generator. This complex includes a small pair of fatty bursae embedded in a pair of connective tissue lips, a cartilaginous blade, a stout ligament, and an array of soft tissue air sacs. Comparing and contrasting the morphologic patterns of nasal structures across species representing every extant odontocete superfamily reveals probable homologous relationships, which suggests that all toothed whales may be making their biosonar signals by a similar mechanism.
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              Comparative Anatomy of the Bony Labyrinth (Inner Ear) of Placental Mammals

              Background Variation is a naturally occurring phenomenon that is observable at all levels of morphology, from anatomical variations of DNA molecules to gross variations between whole organisms. The structure of the otic region is no exception. The present paper documents the broad morphological diversity exhibited by the inner ear region of placental mammals using digital endocasts constructed from high-resolution X-ray computed tomography (CT). Descriptions cover the major placental clades, and linear, angular, and volumetric dimensions are reported. Principal Findings The size of the labyrinth is correlated to the overall body mass of individuals, such that large bodied mammals have absolutely larger labyrinths. The ratio between the average arc radius of curvature of the three semicircular canals and body mass of aquatic species is substantially lower than the ratios of related terrestrial taxa, and the volume percentage of the vestibular apparatus of aquatic mammals tends to be less than that calculated for terrestrial species. Aspects of the bony labyrinth are phylogenetically informative, including vestibular reduction in Cetacea, a tall cochlear spiral in caviomorph rodents, a low position of the plane of the lateral semicircular canal compared to the posterior canal in Cetacea and Carnivora, and a low cochlear aspect ratio in Primatomorpha. Significance The morphological descriptions that are presented add a broad baseline of anatomy of the inner ear across many placental mammal clades, for many of which the structure of the bony labyrinth is largely unknown. The data included here complement the growing body of literature on the physiological and phylogenetic significance of bony labyrinth structures in mammals, and they serve as a source of data for future studies on the evolution and function of the vertebrate ear.
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                Author and article information

                Journal
                Biology Letters
                Biol. Lett.
                The Royal Society
                1744-9561
                1744-957X
                April 12 2016
                April 12 2016
                : 12
                : 4
                : 20160060
                Article
                10.1098/rsbl.2016.0060
                4881348
                27072406
                ce26aa3c-3ca8-47ab-a960-f32be0fe06ca
                © 2016
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