Evolution of a Multiple Sex-Chromosome System by Three-Sequential Translocations among Potential Sex-Chromosomes in the Taiwanese Frog Odorrana swinhoana

Ikuo Miura; Foyez Shams; Si-Min Lin; Marcelo de Bello Cioffi; Thomas Liehr; Ahmed Al-Rikabi; Chiao Kuwana; Kornsorn Srikulnath; Yuya Higaki; Tariq Ezaz

doi:10.3390/cells10030661

Evolution of a Multiple Sex-Chromosome System by Three-Sequential Translocations among Potential Sex-Chromosomes in the Taiwanese Frog Odorrana swinhoana

Cells. 2021 Mar 16;10(3):661. doi: 10.3390/cells10030661.

Authors

Ikuo Miura^{1

2}, Foyez Shams², Si-Min Lin^{1

3}, Marcelo de Bello Cioffi⁴, Thomas Liehr⁵, Ahmed Al-Rikabi⁵, Chiao Kuwana⁶, Kornsorn Srikulnath^{1

7}, Yuya Higaki⁶, Tariq Ezaz^{1

2}

Affiliations

¹ Amphibian Research Center, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima 739-8526, Japan.
² Center for Conservation Ecology and Genomics, University of Canberra, Canberra, ACT 2601, Australia.
³ School of Life Sciences, National Taiwan Normal University, No. 88, Sec. 4, Tingzhou Road, Tapei 116, Taiwan.
⁴ Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos 13565-090, SP, Brazil.
⁵ Institute of Human Genetics, University Hospital Jena, Am Klinikum 1, 07747 Jena, Germany.
⁶ Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan.
⁷ Department of Genetics, Faculty of Science, Kasetsart University, 50 Ngam Wong Wan, Lat Yao, Chatuchak, Bangkok 10900, Thailand.

Abstract

Translocation between sex-chromosomes and autosomes generates multiple sex-chromosome systems. It happens unexpectedly, and therefore, the evolutionary meaning is not clear. The current study shows a multiple sex chromosome system comprising three different chromosome pairs in a Taiwanese brown frog (Odorrana swinhoana). The male-specific three translocations created a system of six sex-chromosomes, ♂X₁Y₁X₂Y₂X₃Y₃-♀X₁X₁X₂X₂X₃X₃. It is unique in that the translocations occurred among three out of the six members of potential sex-determining chromosomes, which are known to be involved in sex-chromosome turnover in frogs, and the two out of three include orthologs of the sex-determining genes in mammals, birds and fishes. This rare case suggests sex-specific, nonrandom translocations and thus provides a new viewpoint for the evolutionary meaning of the multiple sex chromosome system.

Keywords: autosome; fusion; hexavalent; sex-chromosome turnover.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Evolution, Molecular*
Female
Male
Meiosis*
Ranidae / genetics*
Sex Determination Processes*
Translocation, Genetic*
X Chromosome*
Y Chromosome*

Grants and funding

No. 19K06788/the Ministry of Education, Culture, Sports, Science, and Technology of Japan