Evolvability of inner and middle ears in birds and mammals

The vertebrate ear is a remarkable structure. Tightly encapsulated within the densest bone of the skeleton, it comprises the smallest elements of the vertebrate skeleton (auditory ossicles) and gives rise to several different senses: balance, posture control, gaze stabilization, and hearing. Nowhere else in the vertebrate skeleton are different functional units packed so close together and jointly embedded in its skeletal environment, which also hampers the independent evolution of the ear components. Even the growth pattern of the ear deviates from that of the remaining skeleton: In humans and other mammals, the inner and middle ears achieve their final size already before or early after birth, which further challenges evolutionary change. All this makes it puzzling how mammals, as a predominantly nocturnal group reliant on hearing, were able to occupy such a vast diversity of environments in the aquatic, terrestrial, subterranean, and aerial realms that require an amazing disparity not only in hearing abilities, but also in locomotion and posture. How could the different, tightly connected parts of the ear adapt independently to these diverse functional and environmental regimes? Despite its similar function, the ear is composed of different bones in mammals, birds, and reptiles. In birds and reptiles, the lower jaw and its joint are composed of multiple bones, and they have a single auditory ossicle that transmits the sound. Modern mammals, by contrast, have three ossicles (malleus, incus, stapes), all of which are separate from the jaw. This evolutionary transformation of the primary jaw joint into the mammalian ear ossicles is one of the most iconic transitions in vertebrate evolution, but it is not clear why this complex transition has happened. We propose that this substantial evolutionary change of mammalian ear anatomy has in addition to any direct enhancements of mastication and hearing also increased the "evolvability" (capacity for adaptive evolution) of the ear and its associated sensory functions. The incorporation of the bones of the primary jaw joint into the ear has considerably increased the genetic, regulatory, and developmental complexity of the mammalian ear. This increase in the number of genetic and developmental factors, in turn, has increased the evolutionary degrees of freedom for an independent adaptation of the different functional units of the ear: the number of genetic and developmental knobs for natural selection to turn. Despite the tight spatial entanglement of functional ear components, the increased evolvability of the mammalian ear may have contributed to the evolutionary success and adaptive diversification of mammals in the vast diversity of ecological and behavioral niches observable today. We will test this hypothesis by comparing the variational properties and adaptive evolution of inner and middle ear shape across birds and mammals, including humans, by modern 3D imaging and statistics.

The vertebrate ear is a remarkable structure. Encapsulated within a very small space and comprising the smallest bones of the skeleton, the vertebrate ear structures are key to several different senses: hearing, balance, posture control, and gaze stabilization. The transformation of the primary jaw joint into the middle ear ossicles in mammals is one of the most iconic transitions in vertebrate evolution, but the drivers of this complex evolutionary trajectory remain largely unknown. In the project we assessed a novel hypothesis: The incorporation of the bones of the primary jaw joint into the middle ear has increased the genetic and developmental complexity of the ear in mammals, which may have increased the evolutionary degrees of freedom for independent adaptations of the different functional units of the ear, thus fostering the vast behavioural and ecological disparity encountered in mammals. This increased "evolvability" of the mammalian ear may have contributed to the evolutionary success and adaptive diversification of mammals. We tested this hypothesis by comparing the variational properties and adaptive evolution of inner and middle ear shape across birds and mammals, including humans. In a 2024 paper published in Nature Communications, we focused on Afrotheria, a group of related mammals with a vast diversity of anatomies and habitats, such as the aardvark, elephants, golden moles, hyraxes, elephant shrews and sea cows. Using high-resolution CT scans and geometric morphometrics, we compared the shape of the ear in these afrotherians to mammals that are analogous in their morphology, ecology and/or behaviour, but which are only very distantly related to afrotherians, for example dolphins, anteaters and hedgehogs. Using a novel analytic framework, we found that inner ear shape is more similar between analogous species than between non-analogous species, even when non-analogous species are more closely related. For example, the ear shape of sea cows is less similar to that of elephants or hyraxes, closely related afrotherians, than to that of the dolphin, a much more distantly related mammal. We could show that these similarities originate in evolutionary adaptations to similar environments or behaviours. This very detailed convergent evolution documents the high evolvability of the vertebrate ear, despite all the spatial and developmental constraints. The project also involved methodological work to study phylogenetic signals and patterns in complex data, such as the collected geometric morphometric data. In a 2024 paper in Systematic Biology, we presented a new statistical approach for identifying and exploring phylogenetic signal in such complex data, i.e., the "traces" of evolution in the pattern of morphological similarities among species.