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Population genetic structure of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific.

ABSTRACT: Studying population genetics of deep-sea animals helps us understand their history of habitat colonization and population divergence. Here, we report a population genetic study of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) widely distributed in chemosynthesis-based ecosystems in the Northwest Pacific. Three mitochondrial genes (i.e., atp6, cox1, and nad4) and 6,398 genomewide single nucleotide polymorphisms (SNPs) were obtained from 110 individuals from four hydrothermal vents and two methane seeps. When using the three mitochondrial genes, nearly no genetic differentiation was detected for B. platifrons in the Northwest Pacific. Nevertheless, when using SNP datasets, all individuals in the South China Sea (SCS) and three individuals in Sagami Bay (SB) together formed one genetic cluster that was distinct from the remaining individuals. Such genetic divergence indicated a genetic barrier to gene flow between the SCS and the open Northwest Pacific, resulting in the co-occurrence of two cryptic semi-isolated lineages. When using 125 outlier SNPs identified focusing on individuals in the Okinawa Trough (OT) and SB, a minor genetic subdivision was detected between individuals in the southern OT (S-OT) and those in the middle OT (M-OT) and SB. This result indicated that, although under the influence of the Kuroshio Current and the North Pacific Intermediate Water, subtle geographic barriers may exist between the S-OT and the M-OT. Introgression analyses based on these outlier SNPs revealed that Hatoma Knoll in the S-OT represents a possible contact zone for individuals in the OT-SB region. Furthermore, migration dynamic analyses uncovered stronger gene flow from Dai-yon Yonaguni Knoll in the S-OT to the other local populations, compared to the reverse directions. Taken together, the present study offered novel perspectives on the genetic connectivity of B. platifrons mussels, revealing the potential interaction of ocean currents and geographic barriers with adaption and reproductive isolation in shaping their migration patterns and genetic differentiation in the Northwest Pacific.

SUBMITTER: Xu T

PROVIDER: S-EPMC6231483 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe inhabitants of deep-sea hydrothermal vents occupy ephemeral island-like habitats distributed sporadically along tectonic spreading-centers, back-arc basins, and volcanically active seamounts. The majority of vent taxa undergo a pelagic larval phase, and thus varying degrees of geographical subdivision, ranging from no impedance of dispersal to complete isolation, often exist among taxa that span common geomorphological boundaries. Two lineages of Bathymodiolus mussels segregate on either side of the Easter Microplate, a boundary that separates the East Pacific Rise from spreading centers connected to the Pacific-Antarctic Ridge.ResultsA recent sample from the northwest flank of the Easter Microplate contained an admixture of northern and southern mitochondrial haplotypes and corresponding alleles at five nuclear gene loci. Genotypic frequencies in this sample did not fit random mating expectation. Significant heterozygote deficiencies at nuclear loci and gametic disequilibria between loci suggested that this transitional region might be a 'Tension Zone' maintained by immigration of parental types and possibly hybrid unfitness. An analysis of recombination history in the nuclear genes suggests a prolonged history of parapatric contact between the two mussel lineages. We hereby elevate the southern lineage to species status as Bathymodiolus antarcticus n. sp. and restrict the use of Bathymodiolus thermophilus to the northern lineage.ConclusionsBecause B. thermophilus s.s. exhibits no evidence for subdivision or isolation-by-distance across its 4000 km range along the EPR axis and Galápagos Rift, partial isolation of B. antarcticus n. sp. requires explanation. The time needed to produce the observed degree of mitochondrial differentiation is consistent with the age of the Easter Microplate (2.5 to 5.3 million years). The complex geomorphology of the Easter Microplate region forces strong cross-axis currents that might disrupt self-recruitment of mussels by removing planktotrophic larvae from the ridge axis. Furthermore, frequent local extinction events in this tectonically dynamic region might produce a demographic sink rather than a source for dispersing mussel larvae. Historical changes in tectonic rates and current patterns appear to permit intermittent contact and introgression between the two species.

Project description:BACKGROUND: Bathymodiolus azoricus is a deep-sea hydrothermal vent mussel found in association with large faunal communities living in chemosynthetic environments at the bottom of the sea floor near the Azores Islands. Investigation of the exceptional physiological reactions that vent mussels have adopted in their habitat, including responses to environmental microbes, remains a difficult challenge for deep-sea biologists. In an attempt to reveal genes potentially involved in the deep-sea mussel innate immunity we carried out a high-throughput sequence analysis of freshly collected B. azoricus transcriptome using gills tissues as the primary source of immune transcripts given its strategic role in filtering the surrounding waterborne potentially infectious microorganisms. Additionally, a substantial EST data set was produced and from which a comprehensive collection of genes coding for putative proteins was organized in a dedicated database, "DeepSeaVent" the first deep-sea vent animal transcriptome database based on the 454 pyrosequencing technology. RESULTS: A normalized cDNA library from gills tissue was sequenced in a full 454 GS-FLX run, producing 778,996 sequencing reads. Assembly of the high quality reads resulted in 75,407 contigs of which 3,071 were singletons. A total of 39,425 transcripts were conceptually translated into amino-sequences of which 22,023 matched known proteins in the NCBI non-redundant protein database, 15,839 revealed conserved protein domains through InterPro functional classification and 9,584 were assigned with Gene Ontology terms. Queries conducted within the database enabled the identification of genes putatively involved in immune and inflammatory reactions which had not been previously evidenced in the vent mussel. Their physical counterpart was confirmed by semi-quantitative quantitative Reverse-Transcription-Polymerase Chain Reactions (RT-PCR) and their RNA transcription level by quantitative PCR (qPCR) experiments. CONCLUSIONS: We have established the first tissue transcriptional analysis of a deep-sea hydrothermal vent animal and generated a searchable catalog of genes that provides a direct method of identifying and retrieving vast numbers of novel coding sequences which can be applied in gene expression profiling experiments from a non-conventional model organism. This provides the most comprehensive sequence resource for identifying novel genes currently available for a deep-sea vent organism, in particular, genes putatively involved in immune and inflammatory reactions in vent mussels.The characterization of the B. azoricus transcriptome will facilitate research into biological processes underlying physiological adaptations to hydrothermal vent environments and will provide a basis for expanding our understanding of genes putatively involved in adaptations processes during post-capture long term acclimatization experiments, at "sea-level" conditions, using B. azoricus as a model organism.

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Population genetic structure of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific.

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