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

Abstract

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...

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

“…From the fossil record it appears that the facial skulls of early cetaceans were bilaterally symmetrical (Fordyce & de Muizon, 2001) or slightly asymmetrical (Fahlke et al, 2011). The Archaeoceti, fully adapted to aquatic life, still had subterminal bony nostrils and paranasal sinuses.…”

“…In these animals, the nostrils had already started to migrate caudalward, leading to more efficient surfacing for breathing between dives. The midline sutures of their skulls were slightly distorted clockwise (Fahlke et al, 2011) but the skull bones of both sides were equal in size and in position relative to the midline suture, as is the case in all fossil and extant baleen whales (van Beneden & Gervais, 1868;Heyning, 1989;Heyning & Mead, 1990). The first toothed whales of the Oligocene with their caudal position of the bony nostrils and a facial depression (indicative of a melon and thus the the nose of the sperm whaleability to echolocate (Geisler et al, 2014)) started to shift the bony nares slightly to the left by means of a stronger broadening of skull roof elements on the right (and to twist the area clockwise in dorsal view) (Fordyce & de Muizon, 2001).…”

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

“…Because of this, we have not been able to establish whether the earliest mysticetes retained the primitive low-frequency hearing of archaeocetes, or initially evolved high-frequency hearing like odontocetes, which was subsequently lost. The latter has been suggested by studies based on the presence of a large mandibular foramen, asymmetry in basilosaurid skulls, analyses of basilosaurid cochlear morphology and ancestral state reconstructions from molecular phylogenies [5,[9][10][11]. For the first time, we describe the cochlear anatomy of toothed archaic mysticetes using micro-computed tomography (microCT) of periotic bones representing Mammalodontidae (Museums…”

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

“…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.…”