Bat laryngeal echolocation is considered as one of the most complex and diverse modes of auditory sensory perception in animals and its evolutionary history has been the cause of many scientific controversies in the past two decades. To date, the majority of scientific evidence supports that bats (Chiroptera) are divided into two subordinal groups: Yinpterochiroptera, containing the laryngeal echolocating superfamily Rhinolophidae as sister taxa to the non-laryngeal echolocating family Pteropodidae; and Yangochiroptera, containing all other laryngeal echolocating lineages. This topology has led to an unanswered question in mammalian biology: was laryngeal echolocation lost in the ancestral pteropodids or gained convergently in the echolocating bat lineages? To date, there is insufficient and conflicting evidence from fossil, genomic, morphological and phylogenomic data to resolve this question. We detail an ontogenetic study of fetal cochlear development from seven species of bats and five outgroup mammals and show that in early fetal development, all bats including the non-laryngeal echolocating pteropodids have a similarly large cochlea typically associated with laryngeal echolocation abilities. The subsequent cochlear growth rate in the pteropodids is the slowest of all mammals and leads to the pteropodids and the non-echolocating lineages eventually sharing a similar cochlear morphospace as adults. The results suggest that pteropodids maintain a vestigial developmental stage indicative of past echolocation capabilities and thus support a single origin of laryngeal echolocation in bats.
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Wanninger, A. Morphology is dead — long live morphology! Integrating MorphoEvoDevo into molecular EvoDevo and phylogenomics. Front. Ecol. Evol. 3, 54 (2015).
Springer, M. S., Teeling, E. C., Madsen, O., Stanhope, M. J. & de Jong, W. W. Integrated fossil and molecular data reconstruct bat echolocation. Proc. Natl Acad. Sci. USA 98, 6241–6246 (2001).
Jones, G. Echolocation. Curr. Biol. 15, R484–R488 (2005).
Jones, G., Teeling, E. C. & Rossiter, S. J. From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats. Front. Physiol. 4, 117 (2013).
Teeling, E. C., Jones, G. M. & Rossiter, S. J. in Bat Bioacoustics (eds Fenton, B. et al. ) 25–54 (Springer, 2016).
Simmons, N. B. in Mammal Species of the World: a Taxonomic and Geographic Reference Vol. 1 (eds Wilson, D. E. & Reeder, D. M. ) 312–529 (Johns Hopkins Univ. Press, 2005).
Fenton, M. B. in Bat Evolution, Ecology, and Conservation (eds Adams, R. A. & Pedersen, S. C. ) 47–70 (Springer, 2013).
Teeling, E. C. Hear, hear: the convergent evolution of echolocation in bats? Trends Ecol. Evol. 24, 351–354 (2009).
Springer, M. S. Phylogenetics: bats united, microbats divided. Curr. Biol. 23, R999–R1001 (2013).
Hutcheon, J. M., Kirsch, J. A. & Pettigrew, J. D. Base-compositional biases and the bat problem. III. The questions of microchiropteran monophyly. Phil. Trans. R. Soc. Lond. B 353, 607–617 (1998).
Van Den Bussche, R. A. & Hoofer, S. R. Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxa. J. Mamm. 85, 321–330 (2004).
Teeling, E. C. et al. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307, 580–584 (2005).
Teeling, E. C. et al. Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403, 188–192 (2000).
Meredith, R. W. et al. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011).
Tsagkogeorga, G., Parker, J., Stupka, E., Cotton, J. A. & Rossiter, S. J. Phylogenomic analyses elucidate the evolutionary relationships of bats. Curr. Biol. 23, 2262–2267 (2013).
Li, G., Wang, J., Rossiter, S. J., Jones, G. & Zhang, S. Accelerated FoxP2 evolution in echolocating bats. PLoS ONE 2, e900 (2007).
Zhang, G. et al. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339, 456–460 (2013).
Teeling, E. C., Dool, S. & Springer, M. S. in Evolutionary History of Bats: Fossils, Molecules and Morphology (eds Gunnell, G. F. & Simmons, N. B. ) 1–22 (Cambridge Univ. Press, 2012).
Simmons, N. B., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821 (2008).
Veselka, N. et al. A bony connection signals laryngeal echolocation in bats. Nature 463, 939–942 (2010).
Eiting, T. P. & Gunnell, G. F. Global completeness of the bat fossil record. J. Mamm. Evol. 16, 151–173 (2009).
Gunnell, G. F. & Simmons, N. B. Fossil evidence and the origin of bats. J. Mamm. Evol. 12, 209–246 (2005).
Simmons, N. B., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. Inferring echolocation in ancient bats. Nature 466, E8–E9 (2010).
Habersetzer, J. & Storch, G. Cochlea size in extant Chiroptera and Middle Eocene microchiropterans from Messel. Naturwissenchaften 79, 462–466 (1992).
Thewissen, J. G. et al. Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proc. Natl Acad. Sci. USA 103, 8414–8418 (2006).
Richardson, M. K. & Keuck, G. Haeckel’s ABC of evolution and development. Biol. Rev. 77, 495–528 (2002).
Wang, Z., Han, N., Racey, P. A., Ru, B. H. & He, G. M. A comparative study of prenatal development in Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti . BMC Dev. Biol. 10, 10 (2010).
Cretekos, C. J. et al. Embryonic staging system for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancies in captive-bred animals. Dev. Dynam. 233, 721–738 (2005).
Smaers, J. B. & Rohlf, F. J. Testing species’ deviation from allometric predictions using the phylogenetic regression. Evolution 70, 1145–1149 (2016).
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
This work was supported by grants from the National Natural Science Foundation of China (numbers 31672274 and 31570382) and the Ministry of Science and Technology of the People’s Republic of China (The National Key Research and Development Program, numbers 2016YFD0500300 and 2016YFC1200100).
The authors declare no competing financial interests.
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Wang, Z., Zhu, T., Xue, H. et al. Prenatal development supports a single origin of laryngeal echolocation in bats. Nat Ecol Evol 1, 0021 (2017). https://doi.org/10.1038/s41559-016-0021
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