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      Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents

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          Abstract

          Background

          Chemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge.

          Results

          Both of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5–5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77–1.62%/nucleotide/million years.

          Conclusions

          Our present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-017-0966-3) contains supplementary material, which is available to authorized users.

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          Most cited references67

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          The trouble with isolation by distance.

          The genetic population structure of many species is characterised by a pattern of isolation by distance (IBD): due to limited dispersal, individuals that are geographically close tend to be genetically more similar than individuals that are far apart. Despite the ubiquity of IBD in nature, many commonly used statistical tests are based on a null model that is completely non-spatial, the Island model. Here, I argue that patterns of spatial autocorrelation deriving from IBD present a problem for such tests as it can severely bias their outcome. I use simulated data to illustrate this problem for two widely used types of tests: tests of hierarchical population structure and the detection of loci under selection. My results show that for both types of tests the presence of IBD can indeed lead to a large number of false positives. I therefore argue that all analyses in a study should take the spatial dependence in the data into account, unless it can be shown that there is no spatial autocorrelation in the allele frequency distribution that is under investigation. Thus, it is urgent to develop additional statistical approaches that are based on a spatially explicit null model instead of the non-spatial Island model. © 2012 Blackwell Publishing Ltd.
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            'Everything is everywhere, but, the environment selects'; what did Baas Becking and Beijerinck really say?

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              Advances and limits of using population genetics to understand local adaptation.

              Local adaptation shapes species diversity, can be a stepping stone to ecological speciation, and can facilitate species range expansion. Population genetic analyses, which complement organismal approaches in advancing our understanding of local adaptation, have become widespread in recent years. We focus here on using population genetics to address some key questions in local adaptation: what traits are involved? What environmental variables are the most important? Does local adaptation target the same genes in related species? Do loci responsible for local adaptation exhibit trade-offs across environments? After discussing these questions we highlight important limitations to population genetic analyses including challenges with obtaining high-quality data, deciding which loci are targets of selection, and limits to identifying the genetic basis of local adaptation.
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                Author and article information

                Contributors
                +82-2-3277-4471 , won@ewha.ac.kr
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                30 May 2017
                30 May 2017
                2017
                : 17
                Affiliations
                [1 ]ISNI 0000 0001 2171 7754, GRID grid.255649.9, Interdisciplinary Program of EcoCreative, The Graduate School, , Ewha Womans University, ; Seoul, 03760 Korea
                [2 ]ISNI 0000 0001 2171 7754, GRID grid.255649.9, Division of EcoScience, , Ewha Womans University, ; Seoul, 03760 Korea
                [3 ]ISNI 0000 0004 0400 5538, GRID grid.410913.e, , Division of Polar Life Sciences, Korea Polar Research Institute, ; 26 Songdomirae-ro, Yeonsu-gu, Incheon, 21990 Republic of Korea
                [4 ]ISNI 0000 0001 0116 3029, GRID grid.270056.6, , Monterey Bay Aquarium Research Institute, ; Moss Landing, CA 95039 USA
                Article
                966
                10.1186/s12862-017-0966-3
                5450337
                49c77279-88aa-4529-84a1-aa42bc51a57a
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004230, Korea Polar Research Institute;
                Award ID: PP13040 and PE15050
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: NRF-2015R1A4A1041997
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000085, Directorate for Geosciences;
                Award ID: OCE8917311, OCE9217026, OCE-9529819, OCE9910799, OCE-0241613
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Evolutionary Biology
                chemosynthetic symbiosis,deep-sea hydrothermal vent,bathymodiolus mussels,sulfur-oxidizing endosymbiont,gammaproteobacteria,geographical population structure

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