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The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy

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Abstract

Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogenin (AMEL) genes in cetaceans. AMEL encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy AMELX is functional in enamel-bearing eutherians, whereas the Y-copy AMELY appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in AMELX of mysticetes and four suction feeding odontocetes, Delphinapterus leucas, Monodon monoceros, Kogia breviceps, and Physeter macrocephalus, and in AMELY of mysticetes and odontocetes. Regardless of the functionality, both AMELX and AMELY are equally and unusually small in cetaceans, and even their functional AMELX genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional AMELX and AMELY, both of which are similar to AMELX of Platanista minor. Similar small AMELX and AMELY in archaic cetaceans can be explained by gene conversion between AMELX and AMELY. We speculate that common ancestors of modern cetaceans employed a degenerate AMELX, transferred from a decaying AMELY by gene conversion, at an early stage of their transition to suction feeders.

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Acknowledgments

We are indebted to late Dr. Seiji Ohsumi, a former director of the Institute of Cetacean Research, for providing us with precious samples. We also appreciate Mr. Ken Nakamatsu at the Atmosphere and Ocean Research Institute, the University of Tokyo, for providing us with samples, and Prof. Kenneth M. Weiss and Dr. Anne V. Buchanan at Penn State University for critical reading of this manuscript. K. K. is truly grateful to Prof. Joan T. Richtsmeier at Penn State University for encouragement. This work was made possible by the financial support from the Department of Anthropology at Penn State to K. K., the National Institute of Health (P01HD078233 and R01DE027677) to Prof. Joan T. Richtsmeier, and the JSPS (KAKENHI Grant Number JP12671789) and Nippon Dental University (Research Promotion Grant Number N-17006) to M. I.

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  1. Department of Anthropology, Pennsylvania State University, 409 Carpenter Building, University Park, State College, PA, 16802, USA

    Kazuhiko Kawasaki

  2. Department of Microbiology, School of Life Dentistry at Niigata, The Nippon Dental University, Niigata, Japan

    Masato Mikami

  3. Stock Assessment and Management Division, The Institute of Cetacean Research, Tokyo, Japan

    Mutsuo Goto

  4. Laboratory of Wild Life Science, School of Veterinary Medicine, Kitasato University, Aomori, Japan

    Junji Shindo

  5. Graduate School of Fisheries and Environment Sciences, Nagasaki University, Nagasaki, Japan

    Masao Amano

  6. Department of Histology, School of Life Dentistry at Niigata, The Nippon Dental University, Niigata, Japan

    Mikio Ishiyama

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Kawasaki, K., Mikami, M., Goto, M. et al. The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X–Y Gene Conversion, and Feeding Strategy. J Mol Evol 88, 122–135 (2020). https://doi.org/10.1007/s00239-019-09917-0

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