Infrasonic and Ultrasonic Hearing Evolved after the Emergence of Modern Whales

Abstract

Mysticeti (baleen whales) and Odontoceti (toothed whales) today greatly differ in their hearing abilities: Mysticeti are presumed to be sensitive to infrasonic noises [1-3], whereas Odontoceti are sensitive to ultrasonic sounds [4-6]. Two competing hypotheses exist regarding the attainment of hearing abilities in modern whales: ancestral low-frequency sensitivity [7-13] or ancestral high-frequency sensitivity [14, 15]. The significance of these evolutionary scenarios is limited by the undersampling of both early-diverging cetaceans (archaeocetes) and terrestrial hoofed relatives of cetaceans (non-cetacean artiodactyls). Here, we document for the first time the bony labyrinth, the hollow cavity housing the hearing organ, of two species of protocetid whales from Lutetian deposits (ca. 46-43 Ma) of Kpogamé, Togo. These archaeocete cetaceans, which are transitional between terrestrial and aquatic forms, prove to be a key for determining the hearing abilities of early whales. We propose a new evolutionary picture for the early stages of this history, based on qualitative and quantitative studies of the cochlear morphology of an unparalleled sample of extant and extinct land artiodactyls and cetaceans. Contrary to the hypothesis that archaeocetes have been more sensitive to high-frequency sounds than their terrestrial ancestors [15], we demonstrate that early cetaceans presented a cochlear functional pattern close to that of their terrestrial relatives, and that specialization for infrasonic or ultrasonic hearing in Mysticeti or Odontoceti, respectively, instead only occurred in fully aquatic whales, after the emergence of Neoceti (Mysticeti+Odontoceti).

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

“…Therefore, within cetaceans, infrasonic hearing can be regarded as a purely mysticete trait, and ultrasonic hearing as an odontocete trait. Also, Mourlam and Orliac (2017) concluded that infrasonic and ultrasonic hearing evolved after the emergence of fully aquatic whales and within Neoceti, which contrasts with previous results of infrasonic sensitivity in basilosaurids (Ekdale, 2016;Park et al, 2017). However, no archaeocetes were included in our study, and a more detailed interpretation would be merely speculative based on our data.…”

Reduction of olfactory and respiratory turbinates in the transition of whales from land to sea: the semiaquatic middle Eocene Aegyptocetus tarfa

“…A. tarfa , like other protocetids, was considered able to hear high sonic frequencies, facilitating predation on sound‐producing fish (Bianucci & Gingerich, ; Fahlke et al. ), although a recent study based on the cochlear morphology questioned specialization for ultrasonic hearing among archaeocetes (Mourlam & Orliac, ).…”

Neuroanatomy and inner ear labyrinths of the narwhal, Monodon monoceros, and beluga, Delphinapterus leucas (Cetacea: Monodontidae)

“…; Racicot & Colbert, ; Ekdale & Racicot, ; Racicot et al. ; Mourlam & Orliac, ). Original CT data and 3D *.stl files of the endocasts will be made available through morphosource.org, those scanned at UTCT are available by request from UTCT and digimorph.org staff.…”

“…Two recent studies (Churchill et al. ; Mourlam & Orliac, ) have shown that nine measurements of the inner ear labyrinth in a variety of terrestrial, semi‐aquatic, and fully aquatic mammal groups correspond to hearing sensitivity, such that ultrasonic and infrasonic hearers show clear separation in a principal components analysis (PCA). To visualize the hearing ranges of our selected monodontid species alongside other artiodactyls, we built on these analyses by taking the same measurements as these previous authors, and added them to the PCA performed by Mourlam & Orliac ().…”

“…Various measurements of the cochlea, the primary organ of hearing, correlate with hearing capabilities in mammals (e.g. West, ; Ketten & Wartzok, ), and nine specific measurements have been used recently to investigate hearing ranges across most artiodactyl clades, including cetaceans (Mourlam & Orliac, ). Including our data with previous work allows us to establish probable hearing ranges in M. monoceros .…”