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The biogeographical history of giant earthworms of the Metaphire formosae species group (Clitellata: Megascolecidae) in Taiwan and the Ryukyu Archipelago, with the description of a new species from Yonagunijima, Southern Ryukyus

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Abstract

The non-volant terrestrial fauna of the Ryukyu Archipelago is characterized by high endemism with island groups forming distinct biogeographical regions separated by straits. This endemism has resulted from complex histories of insularization caused by geological events and dispersal through land bridges or across the sea during a timeframe of several million years. However, little is known about the zoogeography of terrestrial invertebrates in this region. We presented the first study looking into the earthworm fauna between Taiwan and the Ryukyu Archipelago under a phylogeographical context, and investigated the systematics and phylogeography of the giant earthworms in the Metaphire formosae species group endemic to this region. We highlighted strong evidence supporting that giant earthworms collected from Yonagunijima, the westernmost island of the Ryukyus, represent a new member of the species group, and further described it as a new species, Metaphire dunan sp. nov. Phylogenetic analyses and divergence time estimation rejected the hypothesis that the separation between M. dunan and its Taiwanese sister species, M. formosae, took place 8 Ma in late Miocene, when Taiwan and the Ryukyu region were supposedly first separated from each other and from the Eurasian continent. Instead, our results suggested that the speciation within the M. formosae species group occurred during the arc-continent collision in Taiwan after 5 Ma and M. dunan diverged from its sister species soon after the diversification of the species group had started. In Taiwan, the divergence of mountain-dwelling species followed a north-to-south pattern, consistent with the southward-propagating arc-continent collision on the island.

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All DNA sequence data reported in this study are available in GenBank.

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Acknowledgements

We appreciate two anonymous reviewers for their constructive comments on an earlier version of this article. We are grateful to Messrs. M. Muramatsu and C. Nemoto of the Education Committee of Yonaguni Town Office for collecting earthworm specimens, to W.-J. Chih and Q.-H. Chen for helping with the laboratory work, to S.-C. Chuang for providing the photo of M. trutina, and to Mr. T. Sasaki, Curator-in-Charge of Fujukan for sending specimens described in Azama and Ishizuka (2018) to Taiwan for the study.

Funding

Funding for this study was supported by the Ministry of Science and Technology, Taiwan (MOST108-2621-B-002–001-MY3) and the Ministry of Education, Taiwan (Yushan Scholar Program) to CHC, by the Taiwan Endemic Species Research Institute to HPS, and by the 21st Century Center of Excellence (COE) program at the University of the Ryukyus to HO.

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Authors and Affiliations

  1. Zoology Division, Endemic Species Research Institute, 1 Ming-shen East Road, Jiji, Nantou, 552, Taiwan

    Huei-Ping Shen

  2. Department of Life Science & Institute of Ecology and Evolutionary Biology, National Taiwan University, 1 Roosevelt Road, Section 4, Taipei, 106, Taiwan

    Chih-Han Chang

  3. Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    Hidetoshi Ota

  4. Institute of Natural and Environmental Sciences, University of Hyogo & Museum of Nature and Human Activities, Yayoigaoka 6, Hyogo, Sanda, 669-1546, Japan

    Hidetoshi Ota

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Conceptualization: CHC and HPS. Sample acquisition: HO. Morphological characterization: HPS. Phylogenetic and biogeographical analyses: CHC. Manuscript writing (first draft): CHC and HPS. Manuscript writing (commenting and editing): CHC, HO and HPS. CHC and HPS contributed equally to the manuscript.

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Shen, HP., Chang, CH. & Ota, H. The biogeographical history of giant earthworms of the Metaphire formosae species group (Clitellata: Megascolecidae) in Taiwan and the Ryukyu Archipelago, with the description of a new species from Yonagunijima, Southern Ryukyus. Org Divers Evol 22, 47–60 (2022). https://doi.org/10.1007/s13127-021-00529-5

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