Hearing from the ocean and into the river: the evolution of the inner ear of Platanistoidea (Cetacea: Odontoceti)

Abstract

The inner ear of the two higher clades of modern cetaceans (Neoceti) is highly adapted for hearing infrasonic (mysticetes) or ultrasonic (odontocetes) frequencies. Within odontocetes, Platanistoidea comprises a single extant riverine representative, Platanista gangetica, and a diversity of mainly extinct marine species from the late Oligocene onward. Recent studies drawing on features including the disparate tympanoperiotic have not yet provided a consensus phylogenetic hypothesis for platanistoids. Further, cochlear morphology and evolutionary patterns have never been reported. Here, we describe for the first time the inner ear morphology of late Oligocene–early Miocene extinct marine platanistoids and their evolutionary patterns. We initially hypothesized that extinct marine platanistoids lacked a specialized inner ear like P. gangetica and thus, their morphology and inferred hearing abilities were more similar to those of pelagic odontocetes. Our results reveal there is no “typical” platanistoid cochlear type, as the group displays a disparate range of cochlear anatomies, but all are consistent with high-frequency hearing. Stem odontocete Prosqualodon australis and platanistoid Otekaikea huata present a tympanal recess in their cochlea, of yet uncertain function in the hearing mechanism in cetaceans. The more basal morphology of Aondelphis talen indicates it had lower high-frequency hearing than other platanistoids. Finally, Platanista has the most derived cochlear morphology, adding to evidence that it is an outlier within the group and consistent with a >9-Myr-long separation from its sister genus Zarhachis. The evolution of a singular sound production morphology within Platanistidae may have facilitated the survival of Platanista to the present day.

Evolution of whale sensory ecology: Frontiers in nondestructive anatomical investigations

“…F I G U R E 1 Composite image showcasing the different aspects of sensory anatomy that can be extracted using nondestructive (here, μCT or HRXCT scanning) means, and how one can exploit the methods to holistically examine sensory anatomy. Data to make visualizations are from: Racicot, Deméré, Beatty, and Boessenecker (2014), Racicot and Rowe (2014), Racicot (2017), Racicot et al (2016), Racicot and Ruf (in prep) Nondestructive μCT has enabled replicable digital measurements and 3DGM analyses describing and comparing the shape of the inner ear across a wide range of taxa both intraspecifically and interspecifically (see, e.g., Aguirre-Fern andez, Mennecart, S anchez-Villagra, S anchez, & Costeur, 2017;Churchill, Martinez-Caceres, de Muizon, Mnieckowski, & Geisler, 2016;Costeur et al, 2018;Ekdale, 2013;Ekdale & Racicot, 2015;Ekdale, 2016b;Galatius et al, 2018;Martins, Park, Racicot, & Cooper, 2020;Mourlam & Orliac, 2017;Orliac, Orliac, Orliac, & Hautin, 2020;Park, Fitzgerald, & Evans, 2016;Park, Evans, Gallagher, & Fitzgerald, 2017;Park, Marx, Fitzgerald, & Evans, 2017;Park et al, 2019;Racicot et al, 2016;Racicot et al, 2018;Racicot et al, 2019;Ritsche et al, 2018;Viglino, Gaet an, Buono, Fordyce, & Park, 2021). Results from this work have established that hearing sensitivities in early, amphibious whales known as protocetids (Protocetidae, Figure 2) were transitional between those of terrestrial artiodactyls and the earliest fully aquatic whales and baleen whales (Mourlam & Orliac, 2017).…”

“…Combining the cochlear information with observations of convergent pathways of maxilla overhang of the frontal in xenorophids contribute to a preferred hypothesis that the apparatus for echolocation may have evolved in parallel in the two related groups (Racicot et al, 2019). Prosqualodon australis and Squalodon calvertensis possessed hearing sensitivity to the high frequency spectrum (Luo & Eastman, 1995;Mourlam & Orliac, 2017;Viglino et al, 2021; Figure 3), but other stem odontocetes, including other simocetids or extinct species more closely related to the crown than xenorophids have not been investigated.…”

“…Among crown odontocetes, extinct and extant platanistoids show a large amount of variation in cochlear morphology suggesting a degree of niche partitioning (Viglino et al, 2021). Additionally, the extant Ganges river dolphin (Platanista gangetica) possesses a uniquely "derived" morphology compared even with other platanistoids (Viglino et al, 2021).…”

“…Among crown odontocetes, extinct and extant platanistoids show a large amount of variation in cochlear morphology suggesting a degree of niche partitioning (Viglino et al, 2021). Additionally, the extant Ganges river dolphin (Platanista gangetica) possesses a uniquely "derived" morphology compared even with other platanistoids (Viglino et al, 2021). Galatius et al (2018) found evidence supporting the hypothesis that larger cetacean predators, such as Acrophyseter deinodon (Lambert, Bianucci, & de Muizon, 2008), drove the convergent evolution of narrow-band high-frequency hearing (NBHF) as a form of acoustic crypsis.…”

“…It seems plausible that echolocation and the associated biosonar apparatus is such an effective sensory modality underwater that selective pressures inevitably lead to it among odontocetes. Prosqualodon and Squalodon were capable of hearing in the higher frequency spectrum (e.g., Mourlam & Orliac, 2017;Viglino et al, 2021), but we have no anatomical information from other parts of the odontocete stem more closely related to crown odontocetes. Crown odontocetes have shown interesting patterns and convergences, particularly for NBHF sound perception (Galatius et al, 2018;Park et al, 2019).…”