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

Ting Xu; Jin Sun; Hiromi K. Watanabe; Chong Chen; Masako Nakamura; Rubao Ji; Dong Feng; Jia Lv; Shi Wang; Zhenmin Bao; Pei Yuan Qian; Jianwen QIU

doi:10.1111/eva.12696

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

Ting Xu, Jin Sun, Hiromi K. Watanabe, Chong Chen, Masako Nakamura, Rubao Ji, Dong Feng, Jia Lv, Shi Wang, Zhenmin Bao, Pei Yuan Qian, Jianwen QIU^*

^*Corresponding author for this work

Department of Biology

Research output: Contribution to journal › Journal article › peer-review

35 Citations (Scopus)

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.

Original language	English
Pages (from-to)	1915-1930
Number of pages	16
Journal	Evolutionary Applications
Volume	11
Issue number	10
DOIs	https://doi.org/10.1111/eva.12696
Publication status	Published - Dec 2018

Scopus Subject Areas

Ecology, Evolution, Behavior and Systematics
Genetics
General Agricultural and Biological Sciences

User-Defined Keywords

Bathymodiolus
deep-sea
genetic structure
introgression
migration patterns
mitochondrial genes
population connectivity
RAD-seq

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10.1111/eva.12696

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@article{8a386eac6fa24b5abbdb03032e1ef4b8,

title = "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.",

keywords = "Bathymodiolus, deep-sea, genetic structure, introgression, migration patterns, mitochondrial genes, population connectivity, RAD-seq",

author = "Ting Xu and Jin Sun and Watanabe, {Hiromi K.} and Chong Chen and Masako Nakamura and Rubao Ji and Dong Feng and Jia Lv and Shi Wang and Zhenmin Bao and Qian, {Pei Yuan} and Jianwen QIU",

note = "Funding Information: Funding information This project was supported by a General Research Fund from University Grants Committee (12302917) and a Strategic Development Fund from Hong Kong Baptist University (15-1012-P04) to JWQ, a HKBU PhD studentship to TX, and an InterRidge Fellowship to JS. We thank the captains and crews of the R/Vs Natsushima, Kaiyo, and Xiangyanghong 9, as well as the pilots and operation teams of the manned deep-submergence vehicle Jiaolong and the ROV Hyper-Dolphin for sampling during the relevant cruises. We thank the principal scientists of the relevant research cruises: Dr. Katsunori Fujikura (JAMSTEC) for the R/V Natsushima cruise NT09-06 leg 1, Dr. Shinsuke Kawagucci (JAMSTEC) for the R/V Kaiyo cruise KY14-02, Dr. Hiroshi Miyake (Kitasato University) for the R/V Kaiyo cruise KY11-02 leg 2, Dr. Hidetaka Nomaki (JAMSTEC) for the R/V Kaiyo cruise KY11-01 leg1, Dr. Ken Takai (JAMSTEC) for the R/V Kaiyo cruise KY14-01, Dr. Hiroyuki Yamamoto (JAMSTEC) for the R/V Natsushima cruise NT13-22, as well as Dr. Feng Liu (COMRA) and Dr. Huaiyang Zhou (Tongji University) for the R/V Xiangyanghong 9 cruise Dayang-31. We also thank Dr. Tadashi Maruyama (JAMSTEC) for his help in establishing collaborations among the co-authors.",

year = "2018",

month = dec,

doi = "10.1111/eva.12696",

language = "English",

volume = "11",

pages = "1915--1930",

journal = "Evolutionary Applications",

issn = "1752-4563",

publisher = "Wiley-Blackwell",

number = "10",

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TY - JOUR

T1 - Population genetic structure of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific

AU - Xu, Ting

AU - Sun, Jin

AU - Watanabe, Hiromi K.

AU - Chen, Chong

AU - Nakamura, Masako

AU - Ji, Rubao

AU - Feng, Dong

AU - Lv, Jia

AU - Wang, Shi

AU - Bao, Zhenmin

AU - Qian, Pei Yuan

AU - QIU, Jianwen

N1 - Funding Information: Funding information This project was supported by a General Research Fund from University Grants Committee (12302917) and a Strategic Development Fund from Hong Kong Baptist University (15-1012-P04) to JWQ, a HKBU PhD studentship to TX, and an InterRidge Fellowship to JS. We thank the captains and crews of the R/Vs Natsushima, Kaiyo, and Xiangyanghong 9, as well as the pilots and operation teams of the manned deep-submergence vehicle Jiaolong and the ROV Hyper-Dolphin for sampling during the relevant cruises. We thank the principal scientists of the relevant research cruises: Dr. Katsunori Fujikura (JAMSTEC) for the R/V Natsushima cruise NT09-06 leg 1, Dr. Shinsuke Kawagucci (JAMSTEC) for the R/V Kaiyo cruise KY14-02, Dr. Hiroshi Miyake (Kitasato University) for the R/V Kaiyo cruise KY11-02 leg 2, Dr. Hidetaka Nomaki (JAMSTEC) for the R/V Kaiyo cruise KY11-01 leg1, Dr. Ken Takai (JAMSTEC) for the R/V Kaiyo cruise KY14-01, Dr. Hiroyuki Yamamoto (JAMSTEC) for the R/V Natsushima cruise NT13-22, as well as Dr. Feng Liu (COMRA) and Dr. Huaiyang Zhou (Tongji University) for the R/V Xiangyanghong 9 cruise Dayang-31. We also thank Dr. Tadashi Maruyama (JAMSTEC) for his help in establishing collaborations among the co-authors.

PY - 2018/12

Y1 - 2018/12

N2 - 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.

AB - 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.

KW - Bathymodiolus

KW - deep-sea

KW - genetic structure

KW - introgression

KW - migration patterns

KW - mitochondrial genes

KW - population connectivity

KW - RAD-seq

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U2 - 10.1111/eva.12696

DO - 10.1111/eva.12696

M3 - Journal article

AN - SCOPUS:85054832103

SN - 1752-4563

VL - 11

SP - 1915

EP - 1930

JO - Evolutionary Applications

JF - Evolutionary Applications

IS - 10

ER -

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

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