Anatomical evidence for low frequency sensitivity in an archaeocete whale: comparison of the inner ear of Zygorhiza kochii with that of crown Mysticeti

Abstract

The evolution of hearing in cetaceans is a matter of current interest given that odontocetes (toothed whales) are sensitive to high frequency sounds and mysticetes (baleen whales) are sensitive to low and potentially infrasonic noises. Earlier diverging stem cetaceans (archaeocetes) were hypothesized to have had either low or high frequency sensitivity. Through CT scanning, the morphology of the bony labyrinth of the basilosaurid archaeocete Zygorhiza kochii is described and compared to novel information from the inner ears of mysticetes, which are less known than the inner ears of odontocetes. Further comparisons are made with published information for other cetaceans. The anatomy of the cochlea of Zygorhiza is in line with mysticetes and supports the hypothesis that Zygorhiza was sensitive to low frequency noises. Morphological features that support the low frequency hypothesis and are shared by Zygorhiza and mysticetes include a long cochlear canal with a high number of turns, steeply graded curvature of the cochlear spiral in which the apical turn is coiled tighter than the basal turn, thin walls separating successive turns that overlap in vestibular view, and reduction of the secondary bony lamina. Additional morphology of the vestibular system indicates that Zygorhiza was more sensitive to head rotations than extant mysticetes are, which likely indicates higher agility in the ancestral taxon.

Ultrasonic hearing and echolocation in the earliest toothed whales

“…Specifically, the cochlea of USNM 534010 possesses several adaptations to high-frequency hearing: reduced number of turns, shorter cochlear length, an extended secondary spiral lamina (relative to mysticetes), a low radii ratio value and reduced overlapping of turns. These features are absent in the low-frequency-sensitive cochleae of archaeocetes and extant mysticetes [17]. The xenorophid represented by USNM 534010 would have therefore possessed a relatively stiff basilar membrane capable of detecting the echo of high-frequency sounds produced in its nasal passages.…”

Relationships of cochlear coiling shape and hearing frequencies in cetaceans, and the occurrence of infrasonic hearing in Miocene Mysticeti

“…The ratio of the most basal and the most apical cochlear turns was determined according to the method as introduced by Manoussaki et al (2008), allowing both turns to have one centrum each, as opposed to a common centrum on the modiolar axis (cf. Chadwick et al, 2006;Ekdale and Racicot, 2015;Ketten et al, 2016). For the determination of the radii of curvature of these turns the line representative of the basilar membrane (derived as described above) was projected in apical view onto an isometric twodimensional (2-D) grid created with MatheKonstruktor (http: //www.martware.de/mathekonstruktor.html, last accessed 14 April 2016).…”

“…There are contrasting hypotheses on the evolution of LF hearing: either dominant LF sensitivity (e.g., Fleischer, 1976a;Nummela et al, 2004;Uhen, 2004;Ekdale and Racicot, 2015;Park et al, 2017) or dominant HF sensitivity (e.g., Ketten, 1992;Fahlke et al, 2011;Churchill et al, 2016) was the ancestral state for all Neoceti (Mysticeti and Odontoceti), implying that LF and infrasonic hearing in Mysticeti is either due to retaining (and improving) the ancestral condition or due to a reduction in HF sensitivity.…”

“…Various methods have been applied to test such a relationship, using either individual variables, and products thereof, such as number of turns and basilar membrane length (West, 1985), the ratio of the radii of the basal and apical turns (Manoussaki et al, 2008), or cochlear shape (Wannaprasert and Jeffery, 2015). However, these methods have either been used in incomparable ways, e.g., radii ratio measured from the modiolar axis Ekdale and Racicot, 2015;Ketten et al, 2016) or using individual spiral centers for each measurement of basal and apical turn (Manoussaki et al, 2008), or they have been applied to a variety of mammals, mainly including hearing generalists (Manoussaki et al, 2008;Wannaprasert and Jeffery, 2015), not shedding much light on hearing in cetaceans in particular. Also, Ketten (1992) and Ketten et al (2016) used basilar membrane width and thickness as correlates for LF sensitivity in whales.…”

“…Also, Ketten (1992) and Ketten et al (2016) used basilar membrane width and thickness as correlates for LF sensitivity in whales. However, soft tissue is not preserved in fossil cochleae, and osteological features that indicate the extent of the basilar membrane, such as the secondary bony lamina, are very delicate and do not preserve well (Ekdale and Racicot, 2015).…”