Evolution of whale sensory ecology: Frontiers in nondestructive anatomical investigations

Abstract

Studies surrounding the evolution of sensory system anatomy in cetaceans over the last ~100 years have shed light on aspects of the early evolution of hearing sensitivities, the small relative size of the organ of balance (semicircular canals and vestibule), brain (endocast) shape and relative volume changes, and ontogenetic development of sensory-related structures. Here, I review advances in our knowledge of sensory system anatomy as informed by the use of nondestructive imaging techniques, with a focus on applied methods in computed tomography (CT and μCT), and identify the key questions that remain to be addressed. Of these, the most important are: Is lower frequency hearing sensitivity the ancestral condition for whales? Did echolocation evolve more than once in odontocetes; and if so, when and why? How has the structure of the cetacean brain changed, through the evolution of whales, and does this correspond to changes in hearing sensitivities? Finally, what are the general pathways of ontogenetic development of sensory systems in odontocetes and mysticetes? Answering these questions will allow us to understand important macroevolutionary patterns in a fully aquatic mammalian group and provides baseline data on species for which we have limited biological information because of logistical limitations.

A well‐preserved cranium from the Judith River Formation (Montana, USA) reveals the inner ear and neuroanatomy of a Campanian baenid turtle

“…Thus, turtle endocasts are relatively poor predictors of brain morphology (Edinger, 1929;Evers et al, 2019;Ferreira et al, 2022;Mautner et al, 2017;Paulina-Carabajal et al, 2013;Wyneken, 2001;Zangerl, 1960). This pattern also holds in certain other vertebrate taxa in which the brain volume does not fill most of the endocranial space, such as squamates (Allemand et al, 2023) and cetaceans (Boessenecker et al, 2017;Ichishima, Kawabe, & Sawamura, 2021;Racicot, 2022), but differs from the relatively good reflection of brain shape by endocast shape in archosaurs (Iwaniuk & Nelson, 2002;Watanabe et al, 2019), many mammals (e.g., De Miguel & Henneberg, 1998Haight & Nelson, 1987;Jerison, 1973;Macrini et al, 2007), and amphibians (Clement et al, 2021). In taxa for which the brain-to-endocranial cavity index is low, the endocast tends to be more cylindrical than the underlying brain (Hopson, 1979;Jerison, 1973;Watanabe et al, 2019).…”

Endocast, brain, and bones: Correspondences and spatial relationships in squamates

“…Cranial endocasts are used to investigate the neuroanatomy of both extant and extinct vertebrates (e.g., Aristide et al, 2019; Benoit et al, 2017; Beyrand et al, 2019; Iwaniuk et al, 2020; Lautenschlager et al, 2018; Lynch & Allen, 2022; Schade et al, 2022; Weisbecker et al, 2021; Zhu et al, 2020). Virtual endocasts, generated by the increasingly widespread use of computed tomographic scanning, provide the potential to track evolution of brain external morphology through deep time, and the possibility to infer cognitive and sensory abilities, as well as behavior, of taxa (e.g., Balanoff & Bever, 2017; Dozo et al, 2022; Holloway et al, 2009; Jerison, 1973; Neubauer, 2014; Racicot, 2021). Nevertheless, despite the capacity of endocranial studies to provide such valuable information, inferring the external brain morphology from an endocast can remain challenging as variable degrees of neuroanatomical resolution may occur depending on taxa.…”

Evolution of ion channels in cetaceans: A natural experiment in the Tree of life

“…3). This category encompasses all aspects of phenotypic changes within the nervous system attributed to the diverse sensory adaptations now thoroughly documented as originating from the transition to aquatic life (Ridgway 1988; Eldridge et al 2022; Racicot 2022; De Vreese et al 2023). These phenotypic changes include modifications in brain morphology, sensory processing, and motor control to support their aquatic lifestyle (Thewissen 2018).…”