Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters

Lilian Lieber; Graham Hall; Jackie Hall; Simon Berrow; Emmett Johnston; Chrysoula Gubili; Jane Sarginson; Malcolm Francis; Clinton Duffy; Sabine P Wintner; Philip D Doherty; Brendan J Godley; Lucy A Hawkes; Matthew J Witt; Suzanne M Henderson; Eleonora de Sabata; Mahmood S Shivji; Deborah A Dawson; David W Sims; Catherine S Jones; Leslie R Noble

doi:10.1038/s41598-020-58086-4

Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters

Lilian Lieber
, Graham Hall
, Jackie Hall
, Simon Berrow
, Emmett Johnston
, Chrysoula Gubili
, Jane Sarginson
, Malcolm Francis
, Clinton Duffy
, Sabine P Wintner
, Philip D Doherty
, Brendan J Godley
, Lucy A Hawkes
, Matthew J Witt
, Suzanne M Henderson
, Eleonora de Sabata
, Mahmood S Shivji
, Deborah A Dawson
, David W Sims
, Catherine S Jones

Leslie R Noble^* (Corresponding Author)

^*Corresponding author for this work

Queen's University Belfast
Manx Basking Shark Watch and Manx Wildlife Trust
Galway - Mayo Institute of Technology
Hellenic Agricultural Organisation, Fisheries Research Institute
Manchester Metropolitan University
National Institute of Water and Atmospheric Research
Department of Conservation, Auckland, New Zealand.
University of KwaZulu-Natal
University of Exeter
Scottish Natural Heritage, Inverness
MedSharks
Nova Southeastern University
University of Sheffield
University of Southampton
Nord University
Nord University

Research output: Contribution to journal › Article › peer-review

26 Citations (Scopus)

22 Downloads (Pure)

Abstract

Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241-830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.

Original language	English
Article number	1661
Number of pages	17
Journal	Scientific Reports
Volume	10
DOIs	https://doi.org/10.1038/s41598-020-58086-4
Publication status	Published - 3 Feb 2020

Bibliographical note

We thank everyone involved in sample collection for their time, expertise and dedication including: Innes Henderson and John McCann; Kevin Robinson and his team from the Cetacean Research and Rescue Unit; Michaél Cottrell, Darren Craig, Laura Kavanagh, Lucy Hunt, Nick Massett and Ian O’Connor; Andrew Brownlow and Nick Davison from the SRUC Wildlife Unit, Inverness; Colin and Louise Speedie of Wave Action and Sealife Surveys (Tobermory); and volunteers from the Manx Basking Shark Watch. Thanks to Margaret Wallace and Giulia Denaro for technical support and Robin Waples as well as Marius Wenzel for data analysis support. JH and GH are grateful to the Manx Wildlife Trust. SB acknowledges funding for fieldwork from the Heritage Council Wildlife Grant (grant reference 16759 and R00342) and the Inishowen Development Partnership. EdeS is grateful to the Prince Albert II of Monaco Foundation for funding Mediterranean fieldwork. DWS was supported by a Marine Biological Association Senior Research Fellowship and acknowledges funding from the Good Gifts Catalogues for sample collection by JH and GH. LRN and CSJ gratefully acknowledge funded access to the Natural Environment Research Council (NERC) Biomolecular Analysis Facility at the University of Sheffield (grant reference NBAF723), as well as funds from Dept. of Environment, Food and Rural Affairs (DEFRA) contract CR0288, and Scottish Natural Heritage (SNH). LL was supported by a studentship from the MASTS (The Marine Alliance for Science and Technology for Scotland) pooling initiative and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

Keywords

EFFECTIVE POPULATION-SIZE
MARINE PREDATOR MOVEMENTS
BASKING SHARKS
PAIRWISE RELATEDNESS
R-PACKAGE
CETORHINUS-MAXIMUS
FORAGING BEHAVIOR
RHINCODON-TYPUS
SOCIAL-BEHAVIOR
WHALE SHARKS

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Cite this

Lieber, L., Hall, G., Hall, J., Berrow, S., Johnston, E., Gubili, C., Sarginson, J., Francis, M., Duffy, C., Wintner, S. P., Doherty, P. D., Godley, B. J., Hawkes, L. A., Witt, M. J., Henderson, S. M., de Sabata, E., Shivji, M. S., Dawson, D. A., Sims, D. W., ... Noble, L. R. (2020). Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters. Scientific Reports, 10, Article 1661. https://doi.org/10.1038/s41598-020-58086-4

Lieber, L, Hall, G, Hall, J, Berrow, S, Johnston, E, Gubili, C, Sarginson, J, Francis, M, Duffy, C, Wintner, SP, Doherty, PD, Godley, BJ, Hawkes, LA, Witt, MJ, Henderson, SM, de Sabata, E, Shivji, MS, Dawson, DA, Sims, DW, Jones, CS & Noble, LR 2020, 'Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters', Scientific Reports, vol. 10, 1661. https://doi.org/10.1038/s41598-020-58086-4

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title = "Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters",

abstract = "Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18\% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241-830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.",

keywords = "EFFECTIVE POPULATION-SIZE, MARINE PREDATOR MOVEMENTS, BASKING SHARKS, PAIRWISE RELATEDNESS, R-PACKAGE, CETORHINUS-MAXIMUS, FORAGING BEHAVIOR, RHINCODON-TYPUS, SOCIAL-BEHAVIOR, WHALE SHARKS",

author = "Lilian Lieber and Graham Hall and Jackie Hall and Simon Berrow and Emmett Johnston and Chrysoula Gubili and Jane Sarginson and Malcolm Francis and Clinton Duffy and Wintner, \{Sabine P\} and Doherty, \{Philip D\} and Godley, \{Brendan J\} and Hawkes, \{Lucy A\} and Witt, \{Matthew J\} and Henderson, \{Suzanne M\} and \{de Sabata\}, Eleonora and Shivji, \{Mahmood S\} and Dawson, \{Deborah A\} and Sims, \{David W\} and Jones, \{Catherine S\} and Noble, \{Leslie R\}",

note = "We thank everyone involved in sample collection for their time, expertise and dedication including: Innes Henderson and John McCann; Kevin Robinson and his team from the Cetacean Research and Rescue Unit; Micha{\'e}l Cottrell, Darren Craig, Laura Kavanagh, Lucy Hunt, Nick Massett and Ian O{\textquoteright}Connor; Andrew Brownlow and Nick Davison from the SRUC Wildlife Unit, Inverness; Colin and Louise Speedie of Wave Action and Sealife Surveys (Tobermory); and volunteers from the Manx Basking Shark Watch. Thanks to Margaret Wallace and Giulia Denaro for technical support and Robin Waples as well as Marius Wenzel for data analysis support. JH and GH are grateful to the Manx Wildlife Trust. SB acknowledges funding for fieldwork from the Heritage Council Wildlife Grant (grant reference 16759 and R00342) and the Inishowen Development Partnership. EdeS is grateful to the Prince Albert II of Monaco Foundation for funding Mediterranean fieldwork. DWS was supported by a Marine Biological Association Senior Research Fellowship and acknowledges funding from the Good Gifts Catalogues for sample collection by JH and GH. LRN and CSJ gratefully acknowledge funded access to the Natural Environment Research Council (NERC) Biomolecular Analysis Facility at the University of Sheffield (grant reference NBAF723), as well as funds from Dept. of Environment, Food and Rural Affairs (DEFRA) contract CR0288, and Scottish Natural Heritage (SNH). LL was supported by a studentship from the MASTS (The Marine Alliance for Science and Technology for Scotland) pooling initiative and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.",

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AU - Lieber, Lilian

AU - Hall, Graham

AU - Hall, Jackie

AU - Berrow, Simon

AU - Johnston, Emmett

AU - Gubili, Chrysoula

AU - Sarginson, Jane

AU - Francis, Malcolm

AU - Duffy, Clinton

AU - Wintner, Sabine P

AU - Doherty, Philip D

AU - Godley, Brendan J

AU - Hawkes, Lucy A

AU - Witt, Matthew J

AU - Henderson, Suzanne M

AU - de Sabata, Eleonora

AU - Shivji, Mahmood S

AU - Dawson, Deborah A

AU - Sims, David W

AU - Jones, Catherine S

AU - Noble, Leslie R

N1 - We thank everyone involved in sample collection for their time, expertise and dedication including: Innes Henderson and John McCann; Kevin Robinson and his team from the Cetacean Research and Rescue Unit; Michaél Cottrell, Darren Craig, Laura Kavanagh, Lucy Hunt, Nick Massett and Ian O’Connor; Andrew Brownlow and Nick Davison from the SRUC Wildlife Unit, Inverness; Colin and Louise Speedie of Wave Action and Sealife Surveys (Tobermory); and volunteers from the Manx Basking Shark Watch. Thanks to Margaret Wallace and Giulia Denaro for technical support and Robin Waples as well as Marius Wenzel for data analysis support. JH and GH are grateful to the Manx Wildlife Trust. SB acknowledges funding for fieldwork from the Heritage Council Wildlife Grant (grant reference 16759 and R00342) and the Inishowen Development Partnership. EdeS is grateful to the Prince Albert II of Monaco Foundation for funding Mediterranean fieldwork. DWS was supported by a Marine Biological Association Senior Research Fellowship and acknowledges funding from the Good Gifts Catalogues for sample collection by JH and GH. LRN and CSJ gratefully acknowledge funded access to the Natural Environment Research Council (NERC) Biomolecular Analysis Facility at the University of Sheffield (grant reference NBAF723), as well as funds from Dept. of Environment, Food and Rural Affairs (DEFRA) contract CR0288, and Scottish Natural Heritage (SNH). LL was supported by a studentship from the MASTS (The Marine Alliance for Science and Technology for Scotland) pooling initiative and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.

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N2 - Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241-830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.

AB - Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241-830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.

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KW - FORAGING BEHAVIOR

KW - RHINCODON-TYPUS

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Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters

Abstract

Bibliographical note

UN SDGs

Keywords

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Catherine Jones

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Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters

Abstract

Bibliographical note

UN SDGs

Keywords

Access to Document

Other files and links

Fingerprint

Profiles

Catherine Jones

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