Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

Thomas M. Vignaud; Jeffrey Allen Maynard; Raphaël Leblois; Mark G. Meekan; Ricardo Vázquez-Juárez; Dení Ramírez-Macías; Simon J. Pierce; David Rowat; Michael L. Berumen; Champak R. Beeravolu; Sandra Baksay; Serge Planes

doi:10.1111/mec.12754

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

Thomas M. Vignaud, Jeffrey Allen Maynard, Raphaël Leblois, Mark G. Meekan, Ricardo Vázquez-Juárez, Dení Ramírez-Macías, Simon J. Pierce, David Rowat, Michael L. Berumen, Champak R. Beeravolu, Sandra Baksay, Serge Planes

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68 Scopus citations

Abstract

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales. © 2014 John Wiley & Sons Ltd.

Original language	English (US)
Pages (from-to)	2590-2601
Number of pages	12
Journal	Molecular Ecology
Volume	23
Issue number	10
DOIs	https://doi.org/10.1111/mec.12754
State	Published - May 14 2014

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: All of the following provided funding for the research presented here (no particular order after the first organization): Labex CORAIL, Ministere de l'Ecologie du Developpement Durable et de l'Energie, Ministere de l'Outre Mer, Fonds Pacifique, IFRECOR, Delegation a la recherche de Polynesie, the Agence Nationale de la Recherche, Institut National de Recherche en Agronomie, the King Abdullah University of Science and Technology, Apache Energy Ltd, SeaWorld Research, Rescue Foundation Inc, Save our Seas Foundation, Australian Institute of Marine Science, Western Australian Department of Parks and Wildlife, EMARNAT-CONACYT, Save Our Seas Foundation, Whale Shark Mexico, Shark Foundation, Rufford Small Grant Foundation and the PADI Foundation. Part of the MIGRAINE work was undertaken using the resources of the INRA MIGALE and GENOTOUL bioinformatics platform and the computing grids of ISEM and CBGP labs. In total, the sampling across all aggregation sites required hundreds of colleagues, students and volunteers. We thank everyone that assisted with sampling.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics

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10.1111/mec.12754

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Vignaud, T. M., Maynard, J. A., Leblois, R., Meekan, M. G., Vázquez-Juárez, R., Ramírez-Macías, D., Pierce, S. J., Rowat, D., Berumen, M. L., Beeravolu, C. R., Baksay, S., & Planes, S. (2014). Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Molecular Ecology, 23(10), 2590-2601. https://doi.org/10.1111/mec.12754

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title = "Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline",

abstract = "This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales. {\textcopyright} 2014 John Wiley & Sons Ltd.",

author = "Vignaud, {Thomas M.} and Maynard, {Jeffrey Allen} and Rapha{\"e}l Leblois and Meekan, {Mark G.} and Ricardo V{\'a}zquez-Ju{\'a}rez and Den{\'i} Ram{\'i}rez-Mac{\'i}as and Pierce, {Simon J.} and David Rowat and Berumen, {Michael L.} and Beeravolu, {Champak R.} and Sandra Baksay and Serge Planes",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: All of the following provided funding for the research presented here (no particular order after the first organization): Labex CORAIL, Ministere de l'Ecologie du Developpement Durable et de l'Energie, Ministere de l'Outre Mer, Fonds Pacifique, IFRECOR, Delegation a la recherche de Polynesie, the Agence Nationale de la Recherche, Institut National de Recherche en Agronomie, the King Abdullah University of Science and Technology, Apache Energy Ltd, SeaWorld Research, Rescue Foundation Inc, Save our Seas Foundation, Australian Institute of Marine Science, Western Australian Department of Parks and Wildlife, EMARNAT-CONACYT, Save Our Seas Foundation, Whale Shark Mexico, Shark Foundation, Rufford Small Grant Foundation and the PADI Foundation. Part of the MIGRAINE work was undertaken using the resources of the INRA MIGALE and GENOTOUL bioinformatics platform and the computing grids of ISEM and CBGP labs. In total, the sampling across all aggregation sites required hundreds of colleagues, students and volunteers. We thank everyone that assisted with sampling.",

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Vignaud, TM, Maynard, JA, Leblois, R, Meekan, MG, Vázquez-Juárez, R, Ramírez-Macías, D, Pierce, SJ, Rowat, D, Berumen, ML, Beeravolu, CR, Baksay, S & Planes, S 2014, 'Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline', Molecular Ecology, vol. 23, no. 10, pp. 2590-2601. https://doi.org/10.1111/mec.12754

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T1 - Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

AU - Vignaud, Thomas M.

AU - Maynard, Jeffrey Allen

AU - Leblois, Raphaël

AU - Meekan, Mark G.

AU - Vázquez-Juárez, Ricardo

AU - Ramírez-Macías, Dení

AU - Pierce, Simon J.

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AU - Beeravolu, Champak R.

AU - Baksay, Sandra

AU - Planes, Serge

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: All of the following provided funding for the research presented here (no particular order after the first organization): Labex CORAIL, Ministere de l'Ecologie du Developpement Durable et de l'Energie, Ministere de l'Outre Mer, Fonds Pacifique, IFRECOR, Delegation a la recherche de Polynesie, the Agence Nationale de la Recherche, Institut National de Recherche en Agronomie, the King Abdullah University of Science and Technology, Apache Energy Ltd, SeaWorld Research, Rescue Foundation Inc, Save our Seas Foundation, Australian Institute of Marine Science, Western Australian Department of Parks and Wildlife, EMARNAT-CONACYT, Save Our Seas Foundation, Whale Shark Mexico, Shark Foundation, Rufford Small Grant Foundation and the PADI Foundation. Part of the MIGRAINE work was undertaken using the resources of the INRA MIGALE and GENOTOUL bioinformatics platform and the computing grids of ISEM and CBGP labs. In total, the sampling across all aggregation sites required hundreds of colleagues, students and volunteers. We thank everyone that assisted with sampling.

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N2 - This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales. © 2014 John Wiley & Sons Ltd.

AB - This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales. © 2014 John Wiley & Sons Ltd.

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Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

Abstract

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ASJC Scopus subject areas

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