Precocial male maturation contributes to the introgression of farmed Atlantic salmon into wild populations

Melissa K. Holborn; Samantha E. Crowley; Steve J. Duffy; Amber M. Messmer; Tony Kess; J. Brian Dempson; Brendan F. Wringe; Ian A. Fleming; Paul Bentzen; Ian R. Bradbury

doi:10.3354/AEI00438

Precocial male maturation contributes to the introgression of farmed Atlantic salmon into wild populations

Melissa K. Holborn, Samantha E. Crowley, Steve J. Duffy, Amber M. Messmer, Tony Kess, J. Brian Dempson, Brendan F. Wringe, Ian A. Fleming, Paul Bentzen, Ian R. Bradbury

Producción científica: Contribución a una revista › Artículo › revisión exhaustiva

3 Citas (Scopus)

Resumen

The escape of domesticated Atlantic salmon Salmo salar from aquaculture facilities represents a continued threat to the genetic and demographic stability of wild salmon stocks. Escaped farm-origin salmon have been shown to hybridize with wild conspecifics, yet the longterm genetic impacts are generally unknown. Theoretically, life history variation, specifically precocial maturation of male hybrids, could fast-track introgression, but evidence for this has been sparse. Here, we used empirical and experimental data to examine the role of precocious male maturation in introgression. We examined hybrid class composition using juvenile sampling and genetic assignment over a 5 yr period following an escape event in southern Newfoundland, a region with high rates of natural male precocial maturation. Initially following the escape, the proportion of first-generation (F1) hybrids was high and then decreased annually, contrasting the proportion of backcross wild individuals, which increased over time. The presence and temporal distribution of backcross wild individuals supports the hypothesis that high rates of precocial maturation can fast-track the long-term impacts of escaped farmed salmon on wild populations via interbreeding. This was experimentally tested using lab-created wild, farmed, and F1 parr released and recaptured from a Newfoundland river to assess levels of precocious male maturation. Observed rates of maturation of F1 hybrids were high and similar to wild parr (77 vs. 73%, respectively), indicating that most F1 hybrids mature precocially. Our results suggest that rates of precocial male maturation should be explicitly considered in risk assessments evaluating the genetic impacts of escaped farmed salmon on wild populations.

Idioma original	English
Páginas (desde-hasta)	205-218
Número de páginas	14
Publicación	Aquaculture Environment Interactions
Volumen	14
DOI	https://doi.org/10.3354/AEI00438
Estado	Published - 2022

Nota bibliográfica

Funding Information:
Acknowledgements. The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, release, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation.

Funding Information:
The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, re - lease, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation.

Publisher Copyright:
© S.E.C, I.A.F., P.B., and Fisheries and Oceans Canada 2022. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited.

ASJC Scopus Subject Areas

Aquatic Science
Water Science and Technology
Management, Monitoring, Policy and Law

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@article{9d9f6bc7ba9346729a88503a5e0647b4,

title = "Precocial male maturation contributes to the introgression of farmed Atlantic salmon into wild populations",

abstract = "The escape of domesticated Atlantic salmon Salmo salar from aquaculture facilities represents a continued threat to the genetic and demographic stability of wild salmon stocks. Escaped farm-origin salmon have been shown to hybridize with wild conspecifics, yet the longterm genetic impacts are generally unknown. Theoretically, life history variation, specifically precocial maturation of male hybrids, could fast-track introgression, but evidence for this has been sparse. Here, we used empirical and experimental data to examine the role of precocious male maturation in introgression. We examined hybrid class composition using juvenile sampling and genetic assignment over a 5 yr period following an escape event in southern Newfoundland, a region with high rates of natural male precocial maturation. Initially following the escape, the proportion of first-generation (F1) hybrids was high and then decreased annually, contrasting the proportion of backcross wild individuals, which increased over time. The presence and temporal distribution of backcross wild individuals supports the hypothesis that high rates of precocial maturation can fast-track the long-term impacts of escaped farmed salmon on wild populations via interbreeding. This was experimentally tested using lab-created wild, farmed, and F1 parr released and recaptured from a Newfoundland river to assess levels of precocious male maturation. Observed rates of maturation of F1 hybrids were high and similar to wild parr (77 vs. 73%, respectively), indicating that most F1 hybrids mature precocially. Our results suggest that rates of precocial male maturation should be explicitly considered in risk assessments evaluating the genetic impacts of escaped farmed salmon on wild populations.",

author = "Holborn, {Melissa K.} and Crowley, {Samantha E.} and Duffy, {Steve J.} and Messmer, {Amber M.} and Tony Kess and Dempson, {J. Brian} and Wringe, {Brendan F.} and Fleming, {Ian A.} and Paul Bentzen and Bradbury, {Ian R.}",

note = "Funding Information: Acknowledgements. The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, release, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation. Funding Information: The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, re - lease, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation. Publisher Copyright: {\textcopyright} S.E.C, I.A.F., P.B., and Fisheries and Oceans Canada 2022. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited.",

year = "2022",

doi = "10.3354/AEI00438",

language = "English",

volume = "14",

pages = "205--218",

journal = "Aquaculture Environment Interactions",

issn = "1869-215X",

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T1 - Precocial male maturation contributes to the introgression of farmed Atlantic salmon into wild populations

AU - Holborn, Melissa K.

AU - Crowley, Samantha E.

AU - Duffy, Steve J.

AU - Messmer, Amber M.

AU - Kess, Tony

AU - Dempson, J. Brian

AU - Wringe, Brendan F.

AU - Fleming, Ian A.

AU - Bentzen, Paul

AU - Bradbury, Ian R.

N1 - Funding Information: Acknowledgements. The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, release, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation. Funding Information: The authors thank staff of the Newfoundland DFO Salmonids section for juvenile tissue sampling. The acquisition of aquaculture salmon baseline samples was facilitated by G. Perry, C. Hendry, DFO Aqua culture section Newfoundland Region, and industry partners Cooke Aquaculture and Northern Harvest Sea Farms. We also thank Shahinur Islam for assistance with the rearing, re - lease, and recapture of the experimental crosses. We also thank the Aquatic Biotechnology Laboratory of the Bedford Institute of Oceanography for SNP genotyping and Ian Paterson at the Marine Gene Probe Lab, Dalhousie University, who assisted with laboratory analysis. Funding was provided through the Program for Aquaculture Regulatory Research of Fisheries and Oceans Canada, the Genomics Research and Development Initiative of Canada, the Natural Sciences and Engineering Research Council of Canada, Ocean and Freshwater Science Contribution Program of Fisheries and Oceans Canada, the Ocean Frontier Institute (award from the Canada First Research Excellent Fund), and the Atlantic Salmon Federation. Publisher Copyright: © S.E.C, I.A.F., P.B., and Fisheries and Oceans Canada 2022. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited.

PY - 2022

Y1 - 2022

N2 - The escape of domesticated Atlantic salmon Salmo salar from aquaculture facilities represents a continued threat to the genetic and demographic stability of wild salmon stocks. Escaped farm-origin salmon have been shown to hybridize with wild conspecifics, yet the longterm genetic impacts are generally unknown. Theoretically, life history variation, specifically precocial maturation of male hybrids, could fast-track introgression, but evidence for this has been sparse. Here, we used empirical and experimental data to examine the role of precocious male maturation in introgression. We examined hybrid class composition using juvenile sampling and genetic assignment over a 5 yr period following an escape event in southern Newfoundland, a region with high rates of natural male precocial maturation. Initially following the escape, the proportion of first-generation (F1) hybrids was high and then decreased annually, contrasting the proportion of backcross wild individuals, which increased over time. The presence and temporal distribution of backcross wild individuals supports the hypothesis that high rates of precocial maturation can fast-track the long-term impacts of escaped farmed salmon on wild populations via interbreeding. This was experimentally tested using lab-created wild, farmed, and F1 parr released and recaptured from a Newfoundland river to assess levels of precocious male maturation. Observed rates of maturation of F1 hybrids were high and similar to wild parr (77 vs. 73%, respectively), indicating that most F1 hybrids mature precocially. Our results suggest that rates of precocial male maturation should be explicitly considered in risk assessments evaluating the genetic impacts of escaped farmed salmon on wild populations.

AB - The escape of domesticated Atlantic salmon Salmo salar from aquaculture facilities represents a continued threat to the genetic and demographic stability of wild salmon stocks. Escaped farm-origin salmon have been shown to hybridize with wild conspecifics, yet the longterm genetic impacts are generally unknown. Theoretically, life history variation, specifically precocial maturation of male hybrids, could fast-track introgression, but evidence for this has been sparse. Here, we used empirical and experimental data to examine the role of precocious male maturation in introgression. We examined hybrid class composition using juvenile sampling and genetic assignment over a 5 yr period following an escape event in southern Newfoundland, a region with high rates of natural male precocial maturation. Initially following the escape, the proportion of first-generation (F1) hybrids was high and then decreased annually, contrasting the proportion of backcross wild individuals, which increased over time. The presence and temporal distribution of backcross wild individuals supports the hypothesis that high rates of precocial maturation can fast-track the long-term impacts of escaped farmed salmon on wild populations via interbreeding. This was experimentally tested using lab-created wild, farmed, and F1 parr released and recaptured from a Newfoundland river to assess levels of precocious male maturation. Observed rates of maturation of F1 hybrids were high and similar to wild parr (77 vs. 73%, respectively), indicating that most F1 hybrids mature precocially. Our results suggest that rates of precocial male maturation should be explicitly considered in risk assessments evaluating the genetic impacts of escaped farmed salmon on wild populations.

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Precocial male maturation contributes to the introgression of farmed Atlantic salmon into wild populations

Resumen

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ASJC Scopus Subject Areas

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