Article

Prenatal development supports a single origin of laryngeal echolocation in bats

  • Nature Ecology & Evolution 1, Article number: 0021 (2017)
  • doi:10.1038/s41559-016-0021
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Abstract

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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Acknowledgements

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).

Author information

Author notes

    • Emma C. Teeling
    •  & Shuyi Zhang

    These authors contributed equally to this work.

Affiliations

  1. Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang 110866, China

    • Zhe Wang
    • , Huiling Xue
    •  & Shuyi Zhang
  2. State Key Laboratory of Estuarine and Coastal Research, Institute of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China

    • Tengteng Zhu
    • , Na Fang
    • , Junpeng Zhang
    •  & Shuyi Zhang
  3. Guangdong Entomological Institute, Guangzhou 510260, China

    • Libiao Zhang
  4. Research Institute of Orthopaedics, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China

    • Jian Pang
  5. School of Biology and Environmental Science and UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland

    • Emma C. Teeling

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Contributions

Z.W. and S.Z. designed the study. T.Z., N.F. and J.P. performed the experiments. Z.W., T.Z., N.F., J.Z. and L.Z. collected the specimens. Z.W., H.X., E.C.T. and S.Z. analysed the data and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Zhe Wang or Emma C. Teeling or Shuyi Zhang.

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