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Parallel evolution of semicircular canal form and sensitivity in subterranean mammals

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Abstract

The vertebrate vestibular system is crucial for balance and navigation, and the evolution of its form and function in relation to species’ lifestyle and mode of locomotion has been the focus of considerable recent study. Most research, however, has concentrated on aboveground mammals, with much less published on subterranean fauna. Here, we explored variation in anatomy and sensitivity of the semicircular canals among 91 mammal species, including both subterranean and non-subterranean representatives. Quantitative phylogenetically informed analyses showed significant widening of the canals relative to radius of curvature in subterranean species. A relative canal width above 0.166 indicates with 95% certainty that a species is subterranean. Fluid–structure interaction modelling predicted that canal widening leads to a substantial increase in canal sensitivity; a reasonably good estimation of the absolute sensitivity is possible based on the absolute internal canal width alone. In addition, phylogenetic comparative modelling and functional landscape exploration revealed repeated independent evolution of increased relative canal width and anterior canal sensitivity associated with the transition to a subterranean lifestyle, providing evidence of parallel adaptation. Our results suggest that living in dark, subterranean tunnels requires good balance and/or navigation skills which may be facilitated by more sensitive semicircular canals.

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Acknowledgements

This research was supported by the Fonds Wetenschappelijk Onderzoek—Vlaanderen by postdoctoral fellowships (Grant No. 12R5118N to J.G. and Grant No. 12I8822N to S.B.) and a research grant (Grant No. 1.5.040.18N to J.G.), by special research funds of the Universiteit Antwerpen (Grant No. GOA-33927 to Peter Aerts and Chris Van Ginneken), by a Royal Society Research Grant (Grant No. RG130110 to E.St.J.S.), and by an Erasmus+ Mobility Fellowship for study (to J.P.). Further, we thank the reviewers for their helpful comments and suggestions, as well as all authors who shared the data that were used in this investigation; Dr Phil Cox, for donating some of our naked mole rat specimens; the Cambridge Biotomography Centre for the use of their scanner; and the Museum of Comparative Zoology, Harvard University and the American Museum of Natural History for sharing data on Morphosource.

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  1. Laboratory of Functional Morphology, University of Antwerp, Antwerp, Belgium

    Jana Goyens, Simon Baeckens & Jasmine Pozzi

  2. Evolution and Optics of Nanostructures Lab, Department of Biology, Ghent University, Ghent, Belgium

    Simon Baeckens

  3. Department of Pharmacology, University of Cambridge, Cambridge, UK

    Ewan St. John Smith

  4. Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK

    Matthew J. Mason

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Correspondence to Jana Goyens.

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The CT scans and 3D models of vestibular systems that were made in this study are available at Morphosource (media IDs 000453798 and 000453802).

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Goyens, J., Baeckens, S., Smith, E.S. et al. Parallel evolution of semicircular canal form and sensitivity in subterranean mammals. J Comp Physiol A 208, 627–640 (2022). https://doi.org/10.1007/s00359-022-01578-7

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