The genetic structures of closely related dragonflies in Yaeyama and Taiwan islands

The Amami, Okinawa region of Japan may be designated a World Heritage Site in July of 2021 based on the recent recommendation from the IUCN. The Iriomote wild cat is a symbolic species of the region, having evolved independently on the island. The area is home to many other highly endemic and unique evolutionary species. A research group comprised mostly of former students of Professor Koji Tojo's Faculty of Science lab of Shinshu University focused on the study of dragonflies, continuing from their previous study of their comparative embryogenesis. About 5,000 species of insects belonging to 26 families of the order Dragonfly are known in the world, but those with some gill-shaped protrusions on the abdomen of the larva are extremely rare. Professor Tojo's lab had been studying the Euphaea yayeyamana and the Bayadera brevicauda of the same Euphaeidae dragonfly family in Japan.

Professor Tojo considers that the abdominal gills of these dragonflies are important traits in the origin of insect wings and have studied embryology and developmental genetics targeting this area. In the process of such study, they noticed an interesting genetic feature that is the subject of this paper. Population genetics theory implies that smaller populations that are fragmented contain less genetic diversity than larger populations. They will have a higher rate of genetic fixation due to inbreeding and random genetic drift. However, the result of their genetic analysis of the mitochondrial DNA COI region revealed that E. yayeyamana (Ishigaki/Iriomote) which inhabits smaller islands, has a higher genetic diversity than E. formosa (Taiwan) which inhabits larger island.

Generally, in a small island environment, the population size remains small, so genetic diversity tends to be kept low. Ishigaki Island and Iriomote Island, which were the targets of this study, are only 1/125 and 1/155 in area, respectively, compared to Taiwan. The scale of the mountainous areas on the island is also very different, with the highest altitudes of Ishigaki Island and Iriomote Island being 469 m and 526 m, respectively, while the highest peak in Taiwan is 3,952 m. As for the habitat of Euphaea dragonflies inhabiting mountainous areas, Taiwan has more diverse environments than Ishigaki and Iriomote.

The speciation of E. yayeyamana in Yaeyama (Ishigaki / Iriomote) and E. formosa in Taiwan is estimated to be about 1.4 million years ago. In addition, this study clarified that the genetic diversity of the E. yayeyamana in Ishigaki and Iriomote is much higher than the genetic diversity of the E. formosa in Taiwan. As a result of wide-ranging and comprehensive sampling and gene analysis on both Ishigaki and Iriomote islands, dispersion was found to have occurred within Ishigaki Island and Iriomote Island, and gene flow within each island is actively occurring. On the other hand, gene flow between islands was not observed, and a large genetic differentiation was observed. In addition, it became clear that in the past, there were at least three dispersals from Ishigaki Island to Iriomote Island. The dispersion between Ishigaki Island and Iriomote Island is probably due to the westerly wind (probably Taiwan ? Iriomote ? Ishigaki). No such sign is observed for dispersion in the opposite direction. In other words, it was found that the genomes of dragonflies unique to Taiwan and the Yaeyama region are engraved with genetic information that strongly reflects the effects of geological history and meteorology.

The results of this study were very surprising. The investigation into the cause of such a genetic structure remains a mystery, but Professor Tojo believes that "in Taiwan, a phenomenon such as the "bottleneck effect" that once caused a significant reduction in population size occurred. On the other hand, on Ishigaki and Iriomote Islands, habitats such as those inhabited by E. yayeyamana have been relatively stable over a wide area of the island. In the northeastern peninsula of Ishigaki Island, the forest environment tends to be small and divided. As a result, genetic diversity is also kept low in this area. Through this research, I became keenly aware of the importance of actually analyzing data without being overwhelmed by prejudice."

Not only is the evolutionary history but the morphological traits are unique to this area, and the group is planning to continue to analyze the genetic structure using various molecular markers in addition to pursuing the relationship between morphogenesis and the genetic basis. While adding the analysis of nuclear DNA, the group have analyzed another region of mitochondrial DNA and would like to re-evaluate the gene flow scale using more sensitive gene markers.

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Acknowledgements: We thank Drs H. Kohno, A. Mizutani (Okinawa Regional Research Center, Tokai University), Mr. H. Uehara (Iriomote Station, Tropical Biosphere Research Center, University of the Ryukyus), Dr. M. Nishikawa (Itano Town, Tokushima), Dr. K. Ishida (Gifu City), Dr. A.T.-S. Lin (Department of Earth Sciences, National Central University, Taiwan), Professor H. Chi (Department of Entomology, National Chug Hsing University, Taiwan), Dr. K. Iizumi (Tropical Agricultural Research Front, Japan International Research Center for Agricultural Sciences), Ms. Y. Watanabe (Nishinomiya City), Mr. H. Yokota (Osaka City), Prof. K. Hoyanagi, Dr. K. Yamada, Mr. T. Kano (Faculty of Science, Shinshu University) and many students of the Department of Entomology, National Chug Hsing University, for their help in collecting specimens. We also thank Dr. R.B. Kuranishi and two reviewers for helpful comments that have improved the manuscript.

Photo Credits: Emi KANKE (graduated Fac. of Science, Shinshu University, Tojo Lab), Kohei SUZUKI (MS from Shinshu University, Tojo Lab), Kazuki SEKINÉ (Assistant Professor, Dept. of Environment, Rissho University, MS and PhD from Shinshu University, Tojo Lab), Tomoya SUZUKI (Kyoto University PD, MS and PhD from Shinshu University, Tojo Lab), Kokichi HATTA (Professor Emeritus Nagoya Womens University, Man-Miao YANG (Professor, Chukyo University Taiwan), Koji TOJO (Shinshu University Faculty of Science, Institute for Mountain Science)

Paper: Emi KANKE, Kohei SUZUKI, Kazuki SEKINÉ, Tomoya SUZUKI, Kokichi HATTA, Man-Miao YANG and Koji TOJO. Unique population genetic structure of two closely related euphaeid damselflies in the Yaeyama and Taiwan Islands (Odonata: Euphaeidae). Biological Journal of the Linnean Society, 2021

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