Sound transmission in archaic and modern whales: Anatomical adaptations for underwater hearing

Abstract

The whale ear, initially designed for hearing in air, became adapted for hearing underwater in less than ten million years of evolution. This study describes the evolution of underwater hearing in cetaceans, focusing on changes in sound transmission mechanisms. Measurements were made on 60 fossils of whole or partial skulls, isolated tympanics, middle ear ossicles, and mandibles from all six archaeocete families. Fossil data were compared with data on two families of modern mysticete whales and nine families of modern odontocete cetaceans, as well as five families of noncetacean mammals. Results show that the outer ear pinna and external auditory meatus were functionally replaced by the mandible and the mandibular fat pad, which posteriorly contacts the tympanic plate, the lateral wall of the bulla. Changes in the ear include thickening of the tympanic bulla medially, isolation of the tympanoperiotic complex by means of air sinuses, functional replacement of the tympanic membrane by a bony plate, and changes in ossicle shapes and orientation. Pakicetids, the earliest archaeocetes, had a land mammal ear for hearing in air, and used bone conduction underwater, aided by the heavy tympanic bulla. Remingtonocetids and protocetids were the first to display a genuine underwater ear where sound reached the inner ear through the mandibular fat pad, the tympanic plate, and the middle ear ossicles. Basilosaurids and dorudontids showed further aquatic adaptations of the ossicular chain and the acoustic isolation of the ear complex from the skull. The land mammal ear and the generalized modern whale ear are evolutionarily stable configurations, two ends of a process where the cetacean mandible might have been a keystone character.

Evolutionary Paths to Mammalian Cochleae

“…Microchiropteran prestins also evolved rapidly during this time and, as noted, developed characteristic molecular features that also evolved independently in toothed whales, whose evolution began much later (about 35 Ma ago;McGowan et al 2009;Zhou et al 2011). These whales were large, of course, but were able to use high frequencies because, as water dwellers, they were able to abandon their "land-lubber" middle ear (Nummela et al 2007), whose frequency response is strongly correlated with body size. New evidence points to a more recent, explosive evolution of oceanic dolphins within the last 11 Ma (McGowan 2011).…”

Shape analysis of odontocete mandibles: Functional and evolutionary implications

“…Over the course of evolution, changes in the hearing apparatus include the loss or reduction of the outer ear pinna and external auditory meatus and extensive restructuring of the mandible. The mandibular foramen has expanded and contains a large mandibular acoustic fat body with uncommon acoustic properties (Norris, 1968;Nummela et al, 2007). In contrast to terrestrial mammals that receive sound through bilaterally paired external pinnae and auditory canals, odontocetes are thought to receive vibrations through multiple pathways.…”

“…The mandibular foramen was present in pakicetids (oldest known whales) and became enlarged in later whales (Thewissen et al, 1996). For example, the foramen is larger in ambulocetids than in the earlier pakicetids (Thewissen et al 1996;Nummela et al, 2007).…”

“…The development of a larger foramen may indicate a development of internal mandibular fat bodies (Nummela et al, 2007). In addition, changes in thickness of the pan bones have occurred.…”

“…In addition, changes in thickness of the pan bones have occurred. The pan bone was relatively thicker in archaeocetes, the ancient whales which gave rise to modern cetaceans, and thinner in extant whales (Thewissen et al, 1996;Nummela et al, 2007). The thinnest portion of the lateral wall, or pan bone, ranges from 1.5mm -3.8mm…”