Dr. R. Benjamin Sulser

Phylogenomics of bats suggests that their echolocation either evolved separately in the bat suborders Yinpterochiroptera and Yangochiroptera, or had a single origin in bat ancestors and was later lost in some yinpterochiropterans1–6. Hearing for echolocation behaviour depends on the inner ear, of which the spiral ganglion is an essential structure. Here we report the observation of highly derived structures of the spiral ganglion in yangochiropteran bats: a trans-otic ganglion with a wall-less Rosenthal’s canal. This neuroanatomical arrangement permits a larger ganglion with more neurons, higher innervation density of neurons and denser clustering of cochlear nerve fascicles7–13. This differs from the plesiomorphic neuroanatomy of Yinpterochiroptera and non-chiropteran mammals. The osteological correlates of these derived ganglion features can now be traced into bat phylogeny, providing direct evidence of how Yangochiroptera differentiated from Yinpterochiroptera in spiral ganglion neuroanatomy. These features are highly variable across major clades and between species of Yangochiroptera, and in morphospace, exhibit much greater disparity in Yangochiroptera than Yinpterochiroptera. These highly variable ganglion features may be a neuroanatomical evolutionary driver for their diverse echolocating strategies4,14–17 and are associated with the explosive diversification of yangochiropterans, which include most bat families, genera and species.

It has long been recognized that, among extant mammals, the afrotherian clade Tenrecomorpha contains an exceptional range of sensory specialists in which arboreal, fossorial, semiaquatic and possibly even echolocating species occur within a single clade. Despite their obvious interest in this regard, the sensory apparatus of these animals has not been investigated with modern techniques. Presented here is a geometric morphometric analysis of virtual endocasts of 24 tenrecomorph species (~ 69% of extant diversity) reconstructed via high-resolution uCT techniques. Utilizing linear regression and PCA analyses we identify a model including allometry, habitat, and evolutionary history as the main factors underlying shape variability. Distinct clusters in the tenrecomorph morphospace correspond to shifts within the olfactory and cortical regions of the brain, which covary with independent evolution of aquatic and fossorial behaviors. These results showcase remarkable instances of sensory convergence within the clade and provide a template for inter- and intra-clade analyses of this distinctive branch of the mammal tree.

Evolutionary theory predicts that sensory systems should adaptively respond to environmental selection. Different ecological niches should, in theory, then correlate with changes in sensory anatomy in lineages that have undergone extensive radiation. The afrotherian clade Tenrecomorpha, comprising of African potamogalines and Malagasy tenrecines, is of particular interest because of its variety: the clade reportedly includes fossorial, arboreal, semiaquatic, and even echolocating taxa. To investigate their sensory ecology, we provide geometric morphometric analyses of inner ear endocasts of 24 tenrec species. We expand this dataset with 9 iodine-stained specimens to study trigeminal organization. Although tenrecomorphs display cross-taxon differences in sensory structures, our analyses distinguish signals of conflicting strength and direction within the tenrec ear, with no single factor that might explain a substantial portion of observed variation when accounting for phylogeny. This contrasts with prior studies of the tenrec cranial endocast, where sensory ecotype and habitat are strongly associated with shape. Iodine-enhanced scans of the trigeminal nerve align with this, and other studies based on bony anatomy. The disparate patterns of shape evolution in Tenrecomorpha and the contrasts exhibited by the inner ear and trigeminal nerve provide a nuanced portrait of neurosensory adaptation, differing from expectations set by other mammalian groups.