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.

Highlights

  • Hydrothermal vents and cold seeps generally occur in tectonically active areas and along continental margins, where neighboring sites are often separated by tens to hundreds of kilometers in the ocean (Le Bris et al, 2016)

  • Values of pairwise FST calculated based on the first outlier single nucleotide polymorphisms (SNPs) dataset containing 106 outlier SNPs ranged from −0.0099 to 0.2785, with statistical significance (p < 0.00001) detected in all pairwise evaluations between the local population of Jiaolong Ridge (JR) and those in the Okinawa Trough (OT)-­ Sagami Bay (SB) region (FST range: 0.1953 to 0.2785) after Bonferroni correction (Supporting Information Table S13)

  • By using genomewide SNPs rather than mitochondrial genes, two cryptic semi-­isolated lineages of B. platifrons in the Northwest Pacific were identified in this study, which may have been formed due to the barrier effect of the Luzon Strait or the contact zone been trapped by it

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Summary

Introduction

Hydrothermal vents and cold seeps generally occur in tectonically active areas and along continental margins, where neighboring sites are often separated by tens to hundreds of kilometers in the ocean (Le Bris et al, 2016). Most marine benthic animals, including those in the deep ocean, have a biphasic life with a pelagic larval stage through which they achieve connectivity across different habitats (Cowen & Sponaugle, 2009). Deep-­sea mussels in the genus Bathymodiolus (Bivalvia: Mytilidae) are one of the most iconic, dominant, and important foundation taxa in chemosynthesis-­based ecosystems (Van Dover, 2000). Dense Bathymodiolus mussel beds generate a highly complex habitat for a variety of other animals to inhabit

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