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Phylogenetic Relationships of Deep-Sea Bathymodiolus Mussels to Their Mytilid Relatives from Sunken Whale Carcasses and Wood

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Phylogenetic Relationships of Deep-Sea Bathymodiolus Mussels to Their Mytilid Relatives from Sunken Whale Carcasses and Wood VENUS 67 (3-4): 123-134, 2009 Review Phylogenetic Relationships of Deep-Sea Bathymodiolus Mussels to their Mytilid Relatives from Sunken Whale Carcasses and Wood Yuko Fujita1, Hiroto Matsumoto1, Yoshihiro Fujiwara2, Jun Hashimoto3, Sergey V. Galkin4, Rei Ueshima5 and Jun-Ichi Miyazaki6* 1Institute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan 2Research Program for Marine Biology and Ecology, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Natsushima, Yokosuka, Kanagawa 237-0061, Japan 3Faculty of Fisheries, Nagasaki University, 1-14 Bunkyo, Nagasaki, Nagasaki 852-8521, Japan 4P. P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Nakhimovsky Pr., 36, Moscow 117218, Russia 5Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan 6Faculty of Education and Human Sciences, University of Yamanashi, Kofu, Yamanashi 400-8510, Japan: *[email protected] Abstract: We have investigated worldwide phylogenetic relationships of deep-sea Bathymodiolus mussels and their mytilid relatives by determining mitochondrial DNA sequences. We review herein their phylogenetic relationships and the evolutionary process deduced from s tudies of described and unidentified species collected recently from vents, seeps, sunken whale carcasses and wood. Phylogenetic analysis of the sequence data together with those from a database showed that the mytilid mussels were divided into six clusters and that the mussels in the subfamily Bathymodiolinae are split into four groups. Neither the subfamily Bathymodiolinae nor the genus Bathymodi olus were monophyletic, suggesting that it is necessary to reevaluate their classification. In the evolutionary process of the conventional Bathymodiolinae, the group including only Tamu fisheri split first, and the basal trichotomous split into the remaining three groups was followed by diversification of bathymodioline mussels in each group. The first group bifurcated into two subgroups, which incl ude Bathymodiolus and Gigantidas species, respectively. The second group was subdivided into three subclusters containing Indo-West Pacific, Atlantic and eastern Pacific species respectively. The third group included two nominal species restricted to the western Pacific. Species obtained from sunken whale carcasses and wood took the outgroup position to the vent/seep mussels with only one exception, Adipicola crypta from whale carcasses. Modiolus modiolus from shallow water was positioned more distantly to the vent/seep mussels. The findings indicate an evolutionary transition from shallow water to vent/seep sites via whale carcass/wood sites, supporting the “Evolutionary stepping stone hypothesis”. Keywords: chemosynthesis-based community, vent, seep, mitochondrial DNA, stepping stone 124 Y. Fujita et al. Introduction Deep-sea mussels of the genus Bathymodiolus (Mytilidae, Bathymodiolinae) are one of the dominant megabenthos elements in chemosynthesis-based communities around hydrothermal vents on spreading ridges and back-arc basins and in cold-water seeps along subduction zones. They rely primarily on chemoautotrophic bacterial endosymbionts for their nutrition, although they have not abandoned fi lter feeding (Fiala-Médioni et al., 1986; Fisher et al., 1988). Genetic differentiation and consequent speciation of deep-sea organisms in the community are caused by a combination both of factors shared by diverse taxa (topography, geological histories, and oceanic currents) and some that are unique to their respective taxa such as dispersal ability, physiology, and settlement cues (Vrijenhoeck, 1 997; Won et al., 2003). Our previous studies (Miyazaki et al., 2004; Iwasaki et al., 2006; Miyazaki et al., 2008; Miyazaki, 2008) showed intraspecific genetic exchanges between populations from the hydrothermal vents of the Okinawa Trough and the cold-water seeps of Sagami Bay (over 1,500 km apart) in two species, B. japonicus and B. platifrons, although these two species do not inhabit the Izu-Ogasa wara Island-arc (ca. 500 km from Sagami Bay). This suggests that colonization and speciation of the two species are not dependent on geographical distances and that larval dispersal ability is relatively high and favorable for colonization of patchy and ephemeral habitats. Hydrothermal vents, emitting water heated by underlying magmatic chambers, persist for only a few decades, supplying inorganic n utrients such as sulfide and methane to chemosynthetic bacteria, while cold-water seeps, exuding water as cold as the ambient deep-sea water, provide a relatively stable source of these materials (Jollivet, 1996). Nevertheless, environmental types (vent vs. seep) are not responsible for habitat segregation and speciation in the two Bathymodiolus species (Iwasaki et al., 2006). Nineteen species of Bathymodiolus mussels have been described since the genus was first proposed (Kenk ＆ Wilson, 1985). Three bathymodioline species belonging to the genera Tamu and Gigantidas have been described (Gustafson et al., 1998; Cosel ＆ Marshall, 2003; Hashimoto ＆ Yamane, 2005). By sequencing of mitochondrial genes, 16 species of Bathymodiolus mussels were clustered into three groups as follows: the first includes four species from Japanese waters and one Atlantic species, the second includes one species from Japanese waters, one western Pacific species, one Indian species, two eastern Pacific species and four Atlantic species, and the third includes one species from Japanese waters and one western Pacific species (Iwasaki et al., 2006). Thereafter, active exploration of new localities and careful surveys of known localities has led to the discovery of many unidentified mussels. Molecular phylogenetics, by analyzing DNA sequences of the unidentified mussels as well as accumulating database sequences, offers a good opportunity to uncover the evolutionary process of Bathymodiolus mussels and their relatives. Phylogenetic relationships of Bathymodiolus mussels and their relatives Specimens used are listed in Table 1 and the collection sites are mapped in Fig. 1. The partial DNA fragments of the mitochondrial COI gene were sequenced from more than five specimens, if available, of each mussel species. Sequence data was deposited in DDBJ, EMBL, and GenBank databases under accession numbers AB255739-AB255743, AB257513-AB257557. No deletions or insertions were found in the COI sequences. Bathymodiolus mussels and their relatives were divided into six major clusters (Fig. 2). Those clusters were marginally or poorly supported. The first cluster (C1) was marginally supported and consisted of the modioline species Benthomodiolus lignicola and Benthomodiolus geikotsucola (Okutani & Miyazaki, 2007) and one unidentified mussels from the Juan de Fuca hydrothermal vents in the eastern Pacific (JdF B. s p.). The latter was previously cited as to Table 1. List of samples. Species Sample no.a Accession no. Sampling site Depth(m) Location Habitat type Dive no.c Bathymodiolinae *Bathymodiolus aduloides AI1 AB170054 Iheya Ridge, Mid-Okinawa Trough 1378 27º33´N; 126º58´E vent 3K#375 * AK1-5 AB170055-059 Off Kikaijima Island 1451 28º26´N; 130º19´E vent 2K#1022 *B. azoricus AZL1 AB170060 Lucky Strike, Mid-Atlantic Ridge 1622-1725 37º17-18´N; 32º17´W vent cruise 47 * AZL2 AB170061 Lucky Strike, Mid-Atlantic Ridge 1622-1725 37º17-18´N; 32º17´W vent cruise 47 #B. brevior B. brevior AY275544 Lau Basin 1750 23º13´S; 176º38´W vent #B. brooksi B. brooksi AY649798 West Florida Escarpment 3314 26º02´N; 84º55´W seep B. childressi ChiG1,2 AB257532-533 Gulf of Mexico 27º44´N; 91º19´W seep dive#4568 Relationships of Deep-Sea Mussels to their Mytilid Relatives *B. hirtus HK1-5 AB170047 Kuroshima Knoll, Off Yaeyama Islands 24º08´N; 124º12´E seep 2K#1370 *B. japonicus JH1,2 AB101423 Off Hatsushima Island, Sagami Bay 35º00´N; 139º14´E seep 2K#715 * JM1-3 AB101422-423 Minami-ensei Knoll, Mid Okinawa Trough 28º24´N; 127º39´E vent 2K#618 *B. marisindicus MK1-5 AB170042-045 Kairei Field, Southern Central Indian Ridge 2454 25º19´S; 70º02´E vent 6K#659 # B. marisindicus AY275543 Edmond, Mid-Indian Ridge 3289 23º53´S; 69º36´E vent #B. mauritanicus B. mauritanicus AY649801 West Africa 1000-1267 0º53´N; 5º28´W seep *B. platifrons PH1-3 AB101419-421 Off Hatsushima Island, Sagami Bay 1180 35º60´N; 139º14´E seep 2K#792 * PH4 AB101421 Off Hatsushima Island, Sagami Bay 1170 35º00´N; 139º14´E seep 2K#715 * PI1,2 AB101421 Iheya Ridge, Mid-Okinawa Trough 1028 27º47´N; 126º54´E vent 2K#863 *B. puteoserpentis PUS1,2 AB170062 Snake Pit, Mid-Atlantic Ridge 3023-3510 23º22´N; 44º56´W vent cruise 47 # B. puteoserpentis AY649796 Snake Pit, Mid-Atlantic Ridge 3023-3510 23º22´N; 44º56´W vent *B. securiformis LK1-5 AB170048-051 Kuroshima Knoll, Off Yaeyama Islands 641 24º88´N; 124º12´E seep 2K#1370 * LA1,2 AB170052-053 Atsumi Knoll, Nankai Trough 1042 33º52´N; 137º23´E seep 2K#1378 *B. septemdierum SM1 AB101424 Myojin Knoll, Izu-Ogasawara Island-arc 1288 32º06´N; 139º52´E vent 2K#1009 * SM2 AB101425 Myojin Knoll, Izu-Ogasawara Island-arc 1290 32º06´N; 139º52´E vent 2K#1115 * SM3-4 AB101426 -427 Myojin Knoll, Izu-Ogasawara Island-arc 1346 32º06´N; 139º52´E vent 2K#1112 * SS1 AB101428 Suiyo Seamount, Izu-Ogasawara Island-arc 1375 28º34´N; 140º39´E vent 2K#627 * SS2,3 AB101429-430 Suiyo Seamount, Izu-Ogasawara Island-arc 1373 28º34´N; 140º39´E vent 2K#889 * SS4 AB170041 Suiyo Seamount, Izu-Ogasawara Island-arc 1373 28º34´N; 140º39´E vent 2K#889 * ST1b AB101425 Hatoma Knoll, Okinawa Trough 1523 24º51´N; 123º50´E vent 2K#1269 * SA1b AB170046 Mariana Back-Arc Basin 3600 18º13´N; 144º42´E vent 6K#357 #B. tangaroa B. tangaroa AY608439 Off Turnagain Cape, New Zealand 920-1205 40º26´S; 178º58´E seep B. thermophilus ThE1 AB257557 9N East Pacific Rise 2524 9º51´N; 104º18´W vent cruise 49 # Bt1 AF456282 11N East Pacific Rise 2515 11º25´N; 103º47´W vent # Bt2 AF456283 13N East Pacific Rise 2228-2229 12º49´N; 103º57´W vent # Bt3 AF456284 Rose Garden, Galapagos Rift 2460 0º48´N; 86º14´W vent # Bt5,6 AF456286-287 7S East Pacific Rise 2746-2747 7º25´S; 107º48-49´W vent Chamorro B. sp. C1-3 AB257530-531 South Chamorro Seamount, Mariana 2899 13º47´N; 146º00´E seep 6K#779 #East Pacific B.
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