MBE Advance Access originally published online on April 27, 2005
Molecular Biology and Evolution 2005 22(7):1543-1545; doi:10.1093/molbev/msi155
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Letter |
Biogeography of Luminous Marine Ostracod Driven Irreversibly by the Japan Current
Research Institute for Cell Engineering, National Institute of Advanced Industrial Science and Technology, Osaka, Japan
E-mail: y-ohmiya{at}aist.go.jp.
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Abstract |
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The biogeography of the luminous marine ostracod Vargula hilgendorfii, also called "Umihotaru," shows that this organism may have arrived relatively recently on the Japanese islands during the final glacier period approximately 10,000 years ago. Phylogenetic relationships also strongly indicate that the Japan Current drove the Umihotaru ostracod northward. It is evident that the Umihotaru ostracod spread rapidly to the major Japanese islands 3,000 km north, whereas its spread was slow in the southwest of the Japanese islands, covering a distance of 400 km. The meandering of the Japan Current, where it passes by the Tokara Gap at 28°N latitude, may be a barrier to Umihotaru ostracod extension.
Key Words: biogeography • genetic divergence • Japan Current • mitochondrial DNA • Okinawa • Ostracoda • refugia
The biogeography of organisms not only helps understand genetic divergence but also permits the estimation and, furthermore, predictions of global or local environmental change (Edmands and Harrison 2003
). Many organisms, including humans, have migrated to Japan via ocean currents or, in the past, over land (Suzuki, Sato, and Ohba 2002). Can the biogeography of a model marine organism estimate or predict to environmental changes around the Japanese islands as an open field? Luminous ostracods are members of the superorder Myodocopa, in the phylum Arthropoda, and are classified into three genera, Vargula, Cypridina, and Conchoecia. The Vargula species inhabits coastal landmasses in the Pacific Ocean and the Caribbean Sea (Morin and Cohen 1991). Shells of what are believed to be ostracods date back to the Ordovician period (500–435 MYA) (Sivete et al. 2003). The Japanese luminous ostracod, Vargula hilgendorfii, also called "Umihotaru," has a body length of about 2–3 mm, large eyes of about 0.2 mm in diameter, and long extending antennae (fig. 1) (Hiruta 1980). Umihotaru are benthonic swimmers and live on the sandy bottom of coastal waters at depths of 0.5–5 m. Active during the night, Umihotaru hide in the sand during the day (Vannier and Abe 1993). Their poor swimming ability limits the extent to which they can spread. They have an ovoviviparous life cycle, in which eggs hatch within the uterus and live young are born. Breeding occurs from spring to autumn in the coastal waters of the major Japanese islands. They do not show characteristic planktonic behavior, even in the juvenile stage, but become adults through five stages and live for about 6 months. It is very easy to collect Umihotaru using a bait trap at night, as they have vigorous appetites and a good sense of smell and sight.
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To clarify the native habitat and geographical extent of the Umihotaru ostracod, we surveyed the southwest to northern regions of the Japanese islands, including Honshu, Kyushu, Shikoku, and Nansei Islands (41°26'N, 141°07' E–24°03'N, 123°46'E), during 1997–2004. This resulted in collected 47 sites (fig. 2A and B, red circle) and 320 sites at which no Umihotaru was collected (fig. 2A and B, blue circle), including those near the collected places. All samples collected were identified as the same species due to their morphological characteristics (Hiruta 1980
), although their size depended on the collecting season, life-cycle stage, or water temperature (data not shown). Although several attempts were made to collect samples, Umihotaru ostracods were not found in the northeast region from 41°26'N, 141°07'E to 36°29'N, 140°37'E where the water temperature is low, even in summer, due to the Okhotsk Current. These results suggest that the Japan Current could be a driving force in the dispersal of Umihotaru ostracods. In addition, no Umihotaru ostracods were found in the vicinity of a rough, rapid-flowing ocean, indicating that a balance between swimming ability and current force may be important to their survival.
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It is difficult to ascertain the evolutionary or biogeographical background of the Myodocopa because they did not easily become fossils (Sivete et al. 2003
). To look at some of their history, we therefore determined the mitochondrial genome sequence of Umihotaru ostracods at Notojima in Honshu Island (Ogoh and Ohmiya 2004). Their mitochondrial genome is 15,926 bp in length, and includes 13 protein-coding genes, 22 transfer RNA genes, and 2 ribosomal RNA genes. On the basis of mitochondrial DNA (mtDNA) sequences, we determined the sequence of the cytochrome b gene from 303 samples of the Umihotaru ostracod collected at 47 sites. The neighbor-joining tree, constructed from a total of 303 sequences (fig. 2C), indicates that there are five major populations: (1) Hateruma, Iriomote, and Taketomi Islands in the Sakishima Islands, (2) Miyako Island, (3) Okinawa Island, (4) Amami Island, and (5) the major islands including Tanageshima, Kyusyu, and Shikoku. The same population occurred in 41 sites around the major islands, including near small islands such as Sado, Oki, and Tsushima, although populations above the 28°N latitude were distributed within a range of about 3,000 km, and two small populations occurred in the Pacific Ocean side (fig. 2A and C, yellow and green in sky blue area). In contrast, in the Nansei Islands, the Umihotaru ostracods form individual populations; for example, a genetic difference occurs between Okinawa and Amami Islands, which are only about 100 km apart. Interestingly, a genetic difference was not observed between ostracods from sites near the Oki and Tsushima Islands, which are about 500 km apart. This indicates that geographical dispersal and genetic relationships differ greatly on the boundary of the 28°N latitude, where the meander of the Japan Current at the Tokara Gap is characterized by a strong and fast flow.
The formation of the present Japanese islands is thought to have occurred since the final glacier period about 10,000 years ago (H. Ujiié and Y. Ujiié 1999). Japanese terrestrial organisms extended across the previously connected islands and some modern-day Japanese organisms can be dated back to at least 70,000 years (Horai 1995). In addition, phylogenetic analysis shows that the freshwater fish Pandaka dates back to 0.7 Myr (Mukai, Suzuki, and Nishida 2004) and the firefly Luciola cruciata to 0.5 Myr (Suzuki, Sato, and Ohba 2002). The history of many marine organisms is not so clear because the ocean provides an open field for the easy exchange of materials and organisms. In this study, we found distinctly different groups of Umihotaru ostracods based on mtDNA at Taketomi, Hateruma, Miyako, and Okinawa Islands, covering a distance of about 300 km, which indicates the divergence of their populations on the Nansei Islands. Based on the date of formation of the present Japanese islands, Umihotaru ostracods should date back to at least 10,000 years. Furthermore, phylogenetic relationships strongly indicate that the Umihotaru ostracods rarely cross the Japan Current near the Tokara Gap. The northward movement of the Japan Current travels around the Japanese islands (fig. 2A and B, red arrows), meanders by the Tokara Gap, and finally divides into two directions, toward the Sea of Japan and the Pacific Ocean, continuing northward. Interestingly, when the Umihotaru ostracod crosses the Tokara Gap, it rapidly spreads about 3,000 km northward, although a small divergent group occurs between the Pacific Ocean and the Sea of Japan coast. This suggests that the present Umihotaru ostracod may be a new race that reached the Japanese islands later than the other present Japanese organisms. Alternatively, it is possible that other types of Umihotaru ostracod existed and died in the Japanese islands before the final glacier period.
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Acknowledgements |
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TOPAbstractAcknowledgementsReferences |
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We thank Y. Nakajima, K. Niwa, K. Kobayashi, C. Suzuki-Ogoh, K. E. Fujimori, N. Wakayama, H. Koutsuka, M. Saika, Y. Henmi, T. Mori, M. Ito, K. Hashimoto, A. Miru, J. Yamazaki, and N. Shikatani for sampling of the Umihotaru ostracod and R. Machida, M. M. Yamauchi, and S. Ohde for technical suggestions.
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Footnotes |
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William Martin, Associate Editor
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References |
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TOPAbstractAcknowledgementsReferences |
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Edmands, S., and J. S. Harrison. 2003. Molecular and quantitative trait variation within and among populations of the intertidal copepod Tigriopus californicus. Evolution 57:2277–2285.[CrossRef][ISI][Medline]
Felsenstein, J. 2000. PHYLIP (phylogeny inference package). Version 3.6. Department of Genetics, University of Washington, Seattle.
Hiruta, S. 1980. Morphology of the larval stages of Vargula hilgendorfii (G. W. Müller) and Euphilomedes nipponica Hiruta from Japan (Ostracoda: Myodocopina). J. Hokkaido Univ. Edu. 30:145–167.
Horai, S. 1995. Evolution and the origins of man: clues from complete sequences of hominoid mitochondrial DNA. Southeast Asian J. Trop. Med. Public Health 26 (Suppl. 1):146–154.
Kimura, M. 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111–120.[CrossRef][ISI][Medline]
Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5:150–163.
Morin, J. G., and A. C. Cohen. 1991. Bioluminescent displays, courtship, and reproduction in ostracodes. Pp. 1–16 in R. Bauer and J. Martin, eds. Crustacean Sexual Biology. Columbia University Press, New York.
Mukai, T., T. Suzuki, and M. Nishida. 2004. Genetic and geographical differentiation of Pandaka gobies in Japan. Ichithyol. Res. 51:222–227.[CrossRef]
Ogoh, K., and Y. Ohmiya. 2004. Complete mitochondrial DNA sequence of the sea-firefly, Vargula hilgendorfii (Crustacea, Ostracoda) with duplicate control regions. Gene 327:131–139.[CrossRef][ISI][Medline]
Sivete, D. J., M. D. Sutton, D. E. Briggs, and D. J. Siveter. 2003. An ostracode crustacean with soft parts from the Lower Silurian. Science 302:1749–1751.
Suzuki, H., Y. Sato, and N. Ohba. 2002. Gene diversity and geographic differentiation in mitochondrial DNA of the Genji firefly, Luciola cruciata (Coleoptera: Lampyridae). Mol. Phylogenet. Evol. 22:193–205.[CrossRef][ISI][Medline]
Ujiié, H., and Y. Ujiié. 1999. Late quaternary course change of the Kuroshio Current in the Ryukyu Arc region, northwestern Pacific Ocean. Mar. Micropaleontol. 37:23–40.
Vannier, J., and K. Abe. 1993. Functional morphology and behavior of Vargula hilgendorfii (Ostracoda: Myodocopa) from Japan, and discussion of its crustacean ectoparasite: preliminary results from video recordings. J. Crust. Biol. 13:51–76.[CrossRef]
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