Echolocation is an active form of orientation in which animals emit sounds and then listen to reflected echoes of those sounds to form images of their surroundings in their brains1. Although echolocation is usually associated with bats, it is not characteristic of all bats2,3. Most echolocating bats produce signals in the larynx, but within one family of mainly non-echolocating species (Pteropodidae), a few species use echolocation sounds produced by tongue clicks4,5. Here we demonstrate, using data obtained from micro-computed tomography scans of 26 species (n = 35 fluid-preserved bats), that proximal articulation of the stylohyal bone (part of the mammalian hyoid apparatus) with the tympanic bone always distinguishes laryngeally echolocating bats from all other bats (that is, non-echolocating pteropodids and those that echolocate with tongue clicks). In laryngeally echolocating bats, the proximal end of the stylohyal bone directly articulates with the tympanic bone and is often fused with it. Previous research on the morphology of the stylohyal bone in the oldest known fossil bat (Onychonycteris finneyi) suggested that it did not echolocate6, but our findings suggest that O. finneyi may have used laryngeal echolocation because its stylohyal bones may have articulated with its tympanic bones. The present findings reopen basic questions about the timing and the origin of flight and echolocation in the early evolution of bats. Our data also provide an independent anatomical character by which to distinguish laryngeally echolocating bats from other bats.
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We thank B. Clare, E. Fraser, B. Galef, L. Jakobsen, D. S. Johnston, L. Lazure, J. McNeil, S. Peters, J. Ratcliffe, D. Riskin, K. Seymour, J. A. Simmons, N. Simmons, J. Szewczak and H. Thewissen for comments on earlier versions of the manuscript, and K. Seymour, who arranged access to the O. finneyi specimen. We are particularly grateful to S. I. Pollmann, who assisted in the preparation of the Supplementary Movies. Our research was supported by an Operating Grant from the Canadian Institutes of Health Research (CIHR MOP-89852), and by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada. The McMaster Bat Lab is also supported by grants from the Canada Foundation for Innovation and the Ontario Innovation Trust.
Author Contributions All authors made essential contributions and helped to write the paper. N.V. and D.D.M. are joint first authors; N.V. was responsible for compiling and analysing the scans and D.D.M. was responsible for making them. D.W.H. provided the facilities for scanning; J.L.E. provided specimens from the Royal Ontario Museum mammals collections; R.K.C. suggested the initial idea of conducting MCT scans of bats and discussed the protocol for matching inner-ear and laryngeal anatomy, M.J.M. and K.L.B. provided expertise about the basicranium and hyoid apparatus in general; P.A.F. provided expertise in echolocation and neurobiology; and M.B.F. provided knowledge of bats and echolocation, and led the writing of the manuscript.
This movie shows the arrangement of the hyoid apparatus in the common vampire bat Desmodus rotundus, a laryngeal echolocator.
This movie shows the arrangement of the hyoid apparatus in the Egyptian fruit bat Rousettus aegyptiacus, a pteropodid that echolocates with tongue clicks.
This movie shows the arrangement of the hyoid apparatus in Blanford's fruit bat Sphaerias blanfordi, a non-echolocating pteropodid.
About this article
Journal of Comparative Physiology A (2018)