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Comparative Population Structure of Two Dominant Species, Shinkaia Crosnieri

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Comparative Population Structure of Two Dominant Species, Shinkaia Crosnieri Comparative population structure of two dominant species, Shinkaia crosnieri (Munidopsidae: Shinkaia) and Bathymodiolus platifrons (Mytilidae: Bathymodiolus), inhabiting both deep-sea vent and cold seep inferred from mitochondrial multi-genes Yanjun Shen1,2,*, Qi Kou3,*, Weitao Chen1,2, Shunping He1, Mei Yang3, Xinzheng Li3 & Xiaoni Gan1 1The Key Laboratory of Aquatic Biodiversity and Conservation of the Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Hubei, China 2University of the Chinese Academy of Sciences, Beijing 100039, China 3Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China Keywords Abstract Chemosynthetic fauna, environmental heterogeneity, genetic diversity, genetic Deep-sea hydrothermal vents and cold seeps, limited environments without isolation, population distribution patterns. sunlight, are two types of extreme habitat for marine organisms. The differences between vents and cold seeps may facilitate genetic isolation and produce popu- Correspondence lation heterogeneity. However, information on such chemosynthetic fauna taxa Xiaoni Gan, The Key Laboratory of Aquatic is rare, especially regarding the population diversity of species inhabiting both Biodiversity and Conservation of the Chinese vents and cold seeps. In this study, three mitochondrial DNA fragments (the Academy of Sciences, Institute of cytochrome c oxidase submit I (COI), cytochrome b gene (Cytb), and 16S) Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Hubei, China were concatenated as a mitochondrial concatenated dataset (MCD) to examine Tel: 027-68780089; the genetic diversity, population structure, and demographic history of Shinkaia Fax: 027-68780071; crosnieri and Bathymodiolus platifrons. The genetic diversity differences between E-mail: [email protected] vent and seep populations were statistically significant for S. crosnieri but not and for B. platifrons. S. crosnieri showed less gene flow and higher levels of genetic Xinzheng Li, Institute of Oceanology, differentiation between the vent and seep populations than B. platifrons.In Chinese Academy of Sciences, addition, the results suggest that all the B. platifrons populations, but only the Qingdao 266071, China Tel: 0532-82898771; S. crosnieri vent populations, passed through a recent expansion or bottleneck. Fax: 0532-82898798; Therefore, different population distribution patterns for the two dominant spe- E-mail: [email protected] cies were detected; a pattern of population differentiation for S. crosnieri and a homogeneity pattern for B. platifrons. These different population distribution Funding Information patterns were related to both extrinsic restrictive factors and intrinsic factors. This work was supported by the Strategic Based on the fact that the two species were collected in almost identical or Priority Research Program of the Chinese adjacent sampling sites, we speculated that the primary factors underlying the Academy of Sciences (nos. XDB060101, XDB06010101 and XDA11020303) and the differences in the population distribution patterns were intrinsic. The historical IOCAS (no. 2012IO060105). demographics, dispersal ability, and the tolerance level of environmental hetero- geneity are most likely responsible for the different distribution patterns. Received: 10 September 2015; Revised: 15 March 2016; Accepted: 21 March 2016 Ecology and Evolution 2016; 6(11): 3571– 3582 doi: 10.1002/ece3.2132 *These authors contributed equally to this work. ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 3571 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Population Structures of Two Deep-Sea Species Y. Shen et al. Introduction have been described beyond 18 species. Only three Bathy- modiolus species in Japanese waters (B. japonicus, Deep-sea hydrothermal vents, first discovered on the B. platifrons, and B. aduloides) are capable of inhabiting Galapagos Rift in the eastern Pacific Ocean in 1977 (Cor- both vents and cold seeps. In particular, the same haplo- liss et al. 1979), are typically located in mid-ocean ridges types have been found to be shared by B. platifrons from and back-arc spreading centers. Vents have extremely distant localities and highly differentiated environments high temperatures, high pressure levels, and high levels of (Miyazaki et al. 2004). Shinkaia crosnieri (Munidopsidae: toxins (Yang et al. 2013). Cold seeps, situated in subduc- Shinkaia) is also considered the dominant member of the tion zones with ecosystems similar to vents, are areas fauna inhabiting many deep-sea hydrothermal vents and where chemically modified fluids derived from hydrocar- minority cold seeps, including Hatoma Knoll, the For- bon reservoirs, methane hydrates, pore waters in sedi- mosa Ridge off southwest Taiwan, and the Okinawa ments, and sites of organic enrichment (such as whale Trough (Chevaldonne and Olu 1996; Tsuchida and Fuji- skeletons) are released into the ocean (Van Dover et al. kura 2000; Watabe and Miyake 2000; Martin and Haney 2002). A few decades ago, sunlight was considered the 2005; Tsuchida et al. 2007). Previous studies of B. plat- essential element for life because photosynthesis provides ifrons from two seeps and one vent revealed no genetic primary production for the biosphere. However, numer- differentiation between the mussel populations of either ous unique “chemosynthetic fauna”, which depend pri- species from cold seeps versus vents and suggested high marily on energy supplied by the chemosynthesis of adaptability to deep-sea chemosynthetic environments bacterial endosymbionts, are found in the limited envi- (Miyazaki et al. 2004). However, the distribution and ronments without sunlight (Tirmizi and Javed 1980; Kenk population structure of S. crosnieri have been reported and Wilson 1985; Hessler and Lonsdale 1991; Kikuchi only at hydrothermal vents in the southern Okinawa and Ohta 1995; Watsuji et al. 2010). Knowledge regarding Trough (Tsuchida et al. 2003). The two dominant species the biological communities around vents and cold seeps (B. platifrons and S. crosnieri) are ideal models as they led to a profound change in our perception of deep-sea exhibit various population distances and inhabit different life (Van Dover et al. 2002). habitat types. Within deep-sea chemosynthetic ecosystems, particu- In this study, three mitochondrial DNA fragments (the larly hydrothermal vents, studies of population structure cytochrome c oxidase submit I (COI), cytochrome b gene and gene flow has recently received much attention for (Cytb), and 16S) were employed as a mitochondrial con- many species, such as giant tubeworms (Hurtado et al. catenated dataset (MCD) to evaluate the genetic diversity, 2004; Coykendall et al. 2011), mussels (Won et al. 2003), genetic structure, and demographic history of B. platifrons swarming shrimp (Teixeira et al. 2012), and provannid and S. crosnieri. The current study also sought to explore gastropods (Kojima et al. 2001; Teixeira et al. 2012). Pop- the adaptability of the two dominant species to different ulation diversity studies are also reported for deep-sea deep-sea chemosynthetic environments. chemosynthetic communities at the methane seeps in the Gulf of Mexico and eastern Atlantic (Carney et al. 2006; Materials and Methods Olu et al. 2010). From these studies, we are beginning to understand the extent of genetic connectivity among The experiments were performed in accordance with the deep-sea populations associated with chemosynthetic recommendations of the Ethics Committee of the Insti- ecosystems. However, few studies have been conducted to tute of Hydrobiology, Chinese Academy of Sciences. The examine the genetic diversity and population structure for policies were enacted according to the Chinese Associa- species inhabiting both vents and cold seeps, especially tion for Laboratory Animal Sciences and the Institutional for the dominant species. As we know, relying on Animal Care and Use Committee (IACUC) protocols. chemoautotrophic bacteria for nutritional support, all known species of macroorganisms in hydrothermal vents Sampling, identification, and DNA and cold seeps are highly specialized for a symbiotic life- extraction style (Cavanaugh 1983; Fialamedioni and Lepennec 1988; Fisher 1990). The differences between the ecosystems of A total of 64 specimens of S. crosnieri from three vents vents and cold seeps may facilitate the genetic isolation of and one cold seep habitat, and 52 specimens of B. plat- species in both environments. Therefore, it is particularly ifrons from two vents and one cold seep habitat were col- important to determine the extent of population differen- lected by the manned submersible “Jiaolong” during June tiation and genetic isolation for these species. 2013 and the ROV “Faxian” during April 2014. All the Bathymodiolus (Mytilidae: Bathymodiolus) mussels, sample information and photographs used in this study which are the dominant species in vents and cold seeps, are provided in Table 1 and the sampling sites are 3572 ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Y. Shen et al. Population Structures of Two Deep-Sea Species Table 1. Information about the samples used in this study. Species Sampling site Depth (m) Location Habitat type Population name N Date Shinkaia crosnieri West of Tori-shima 996.9 27°47.4417540N Vent
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