On the Embryonic Development of the Nasal Turbinals and Their Homology in Bats

Kai Ito; Vuong Tan Tu; Thomas P Eiting; Taro Nojiri; Daisuke Koyabu

doi:10.3389/fcell.2021.613545

On the Embryonic Development of the Nasal Turbinals and Their Homology in Bats

Front Cell Dev Biol. 2021 Mar 23:9:613545. doi: 10.3389/fcell.2021.613545. eCollection 2021.

Authors

Kai Ito¹, Vuong Tan Tu^{2

3}, Thomas P Eiting⁴, Taro Nojiri^{5

6}, Daisuke Koyabu^{7

8

9}

Affiliations

¹ Department of Anatomy, Tissue and Cell Biology, School of Dental Medicine, Tsurumi University, Yokohama, Japan.
² Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Vietnam.
³ Graduate University of Science and Technology, Vietnam Academy of Science and Technology, Hanoi, Vietnam.
⁴ Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT, United States.
⁵ Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan.
⁶ The University Museum, The University of Tokyo, Tokyo, Japan.
⁷ Research and Development Center for Precision Medicine, University of Tsukuba, Tsukuba, Japan.
⁸ Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong.
⁹ Department of Molecular Craniofacial Embryology, Tokyo Medical and Dental University, Tokyo, Japan.

Abstract

Multiple corrugated cartilaginous structures are formed within the mammalian nasal capsule, eventually developing into turbinals. Due to its complex and derived morphology, the homologies of the bat nasal turbinals have been highly disputed and uncertain. Tracing prenatal development has been proven to provide a means to resolve homological problems. To elucidate bat turbinate homology, we conducted the most comprehensive study to date on prenatal development of the nasal capsule. Using diffusible iodine-based contrast-enhanced computed tomography (diceCT), we studied in detail the 3D prenatal development of various bat species and non-bat laurasiatherians. We found that the structure previously identified as "maxilloturbinal" is not the true maxilloturbinal and is only part of the ethmoturbinal I pars anterior. Our results also allowed us to trace the evolutionary history of the nasal turbinals in bats. The turbinate structures are overall comparable between laurasiatherians and pteropodids, suggesting that pteropodids retain the ancestral laurasiatherian condition. The absence of the ethmoturbinal I pars posterior in yangochiropterans and rhinolophoids has possibly occurred independently by convergent evolution.

Keywords: Chiroptera; evo-devo; homology; microCT (μCT); skull.