A comparison of the intraspecific variation of middle and inner ear morphology between selected mammals and birds

The ear of mammals is particularly complex compared to other vertebrates. During the evolution of mammal ancestors, several bones of the lower jaw and its joint changed morphologically, migrated to the cranium and became part of the middle ear apparatus. Mammals therefore have three auditory or middle ear ossicles – the malleus, the incus and the stapes – compared to only one in other vertebrates: the columella (homologous to the stapes). This complex structure, together with the lengthening and coiling of the cochlea of the inner ear, enabled mammals to increase their hearing range, especially towards high frequencies. The inclusion of extra bones in the mammalian middle ear implies the recruitment of an additional pharyngeal arch during embryonic ear development, as well as additional genetic pathways, relative to other vertebrates. We previously proposed that this higher complexity of the mammalian ear facilitates the independent evolution of the different ear elements, thereby increasing the evolvability of the ear. From this we predict that the mammals exhibit increased morphological variability and modularity of the different ear components within species compared to other vertebrates. In other words, the total shape variation of the mammalian ear is expected to decompose into a higher number of independent factors (or dimensions) than in other vertebrates. To test this, we compare inner and middle ear shape variation among a select sample of mammals and birds, two lineages of roughly the same age. Specifically, ear morphology of humans, European red squirrels, common buzzards and house sparrows was obtained from microCT scans. Using 3D geometric morphometrics, we quantify the morphology of the bony labyrinth (osseous moulding of the inner ear) and the middle ear ossicle(s) with a comprehensive set of anatomical and sliding landmarks in a sample of ~30 individuals per species. Using multivariate statistics, we compare the intraspecific patterns of variation and modularity/integration between the inner and middle ear among the four species. Finally, we discuss the implications of our findings for the evolvability of the mammalian compared to the avian ear.