Abstract
Arising from: N. Veselka et al. Nature 463, 939–942 (2010)10.1038/nature08737; Veselka et al. reply
Laryngeal echolocation, used by most living bats to form images of their surroundings and to detect and capture flying prey1,2, is considered to be a key innovation for the evolutionary success of bats2,3, and palaeontologists have long sought osteological correlates of echolocation that can be used to infer the behaviour of fossil bats4,5,6,7. Veselka et al.8 argued that the most reliable trait indicating echolocation capabilities in bats is an articulation between the stylohyal bone (part of the hyoid apparatus that supports the throat and larynx) and the tympanic bone, which forms the floor of the middle ear. They examined the oldest and most primitive known bat, Onychonycteris finneyi (early Eocene, USA4), and argued that it showed evidence of this stylohyal–tympanic articulation, from which they concluded that O. finneyi may have been capable of echolocation. We disagree with their interpretation of key fossil data and instead argue that O. finneyi was probably not an echolocating bat.
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Main
The holotype of O. finneyi shows the cranial end of the left stylohyal resting on the tympanic bone (Fig. 1c–e). However, the stylohyal on the right side is in a different position, the tip of the stylohyal extends beyond the tympanic on both sides of the skull, and both tympanics are crushed. In our opinion, the skull is too deformed to provide evidence of the spatial relationships of these bones in life. Micro-computed tomography (MCT) images of the skull make clear the extent of crushing and fragmentation (Fig. 1b, d). Veselka et al.8 noted that the stylohyal–tympanic contact on the left side might be a taphonomic artefact, but nevertheless favoured the interpretation that O. finneyi was an echolocating bat. Available evidence indicates otherwise.
Four osteological traits have been postulated as indicators of laryngeal echolocation in bats: (1) an enlarged orbicular apophysis on the malleus3,4; (2) an enlarged cochlea3,4,5,6,7; (3) an enlarged paddle-like or bifurcated cranial tip on the stylohyal3,4; and (4) an articulation between the stylohyal and the tympanic8. Studies in other groups (for example, talpid moles9) indicate that large orbicular apophyses may occur in non-echolocating lineages, hence this trait cannot be considered a definitive indicator of echolocation8. However, the hypothesis that relative cochlear size is a good indicator of the echolocation abilities of bats3,4,5,6,7,8 has not been refuted. The cochlea of O. finneyi falls outside the size range seen in living echolocating bats and is similar to the proportionally smaller cochleae of bats that lack laryngeal echolocation4,8, suggesting that it did not echolocate.
Data presented by Veselka et al.8 indicate that cranial expansion of the stylohyal and an articulation between this structure and the tympanic are 100% correlated in extant bats. Previous reports that two families of echolocating bats (Nycteridae and Megadermatidae) lack stylohyal modifications3,4,10,11 overlooked expansions of the stylohyal where it articulates with the tympanic. We found uniform presence of expansion and flattening of the stylohyal in both families. Observed correlations across all extant bat families indicate that this is a definitive marker of laryngeal echolocation, and that expansion and flattening of the cranial stylohyal should be considered a fundamental part of the stylohyal–tympanic articulation rather than an independent feature. In O. finneyi, the stylohyal is rod-like and has no cranial expansion or flattening other than a tiny knob at the proximal end. We hypothesize that this knob might be an ossified, fused typanohyal, which in some non-echolocating bats (for example, Rousettus, Eonycteris12) and insectivores (Echinosorex, Erinaceus13) is connected to the stylohyal by a thin ligament or cartilage; regardless, it is not comparable to the condition seen in any extant echolocating bat. In contrast with Veselka et al.8, we conclude that O. finneyi did not have a stylohyal–tympanic articulation as it clearly lacks one of the definitive components of this feature: a modified stylohyal with an expanded and flattened cranial end.
Reconstructions of behaviours of extinct animals require careful consideration of preservation artefacts in fossils as well as patterns of form and function among extant animals. Our analyses show that the only two unambiguous pieces of evidence available at this time (cochlear size and stylohyal morphology) support the hypothesis that O. finneyi was not an echolocating bat. Because postcranial morphology indicates that O. finneyi could fly and phylogenetic analyses place it on the most basal branch within Chiroptera4, the ‘flight first’ hypothesis for the origin of flight and echolocation in bats3,4 remains the best-supported hypothesis for the origins of these key features.
Methods
Micro-computed tomography (MCT) images of O. finneyi (Fig. 1b–e) were obtained with an MCT apparatus using a special ‘region of interest’ algorithm (RayScan 200 XE, RayScan Technologies). CT data for Myzopoda aurita (Fig. 1a) were provided by the University of Texas CT laboratory. Image processing was done with VGStudio MAX 2.0.1 (Volume Graphics).
References
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Comparative study of fossil and living bats was carried out by N.B.S. and G.F.G. MCT scanning was coordinated by J.H. and interpreted by J.H. and K.L.S. N.B.S. wrote the manuscript with contributions from J.H., K.L.S. and G.F.G.
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Simmons, N., Seymour, K., Habersetzer, J. et al. Inferring echolocation in ancient bats. Nature 466, E8 (2010). https://doi.org/10.1038/nature09219
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DOI: https://doi.org/10.1038/nature09219
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