Captive-bred Atlantic salmon released into the wild have fewer offspring than wild-bred fish and decrease population productivity

O’Sullivan, Ronan James; Aykanat, Tutku; Johnston, Susan E.; Rogan, Ger; Poole, Russell; Prodöhl, Paulo A.; Eyto, Elvira de; Primmer, Craig R.; McGinnity, Philip; Reed, Thomas E.

doi:10.1098/rspb.2020.1671

Cited by 41 publications

(39 citation statements)

References 56 publications

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“…Genetic homogenization reduces one important aspect of intraspecific diversity. It further compromises individual and population fitness by disrupting local adaptations, at least in short to medium term, through the replacement of locally adapted alleles with non-adaptive ones, which is expected to reduce resilience to future environmental changes [ 11 , 21 , 24 ]. Thus, for salmon populations in the Baltic Sea, genetic homogenization has likely resulted in negative biological consequences.…”

Section: Discussionmentioning

confidence: 99%

“…While in some cases such interventions may be beneficial for assisting threatened populations, a number of genetic conservation concerns have been identified (fitness reductions, reduced effective population size, reduced fitness of recipient populations, etc.) that depend on how artificial propagation and stocking is carried out [11,[21][22][23][24]. Several studies have also documented GH of native populations due to large-scale interbreeding with hatchery strains, including decreases in genetic structuring and isolation by distance (IBD) relationships [25][26][27][28][29].…”

Section: Introductionmentioning

confidence: 99%

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A century of genetic homogenization in Baltic salmon—evidence from archival DNA

Palm

Gilbey

Spong³

et al. 2021

Proc. R. Soc. B.

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Intra-species genetic homogenization arising from anthropogenic impacts is a major threat to biodiversity. However, few taxa have sufficient historical material to systematically quantify long-term genetic changes. Using archival DNA collected over approximately 100 years, we assessed spatio-temporal genetic change in Atlantic salmon populations across the Baltic Sea, an area heavily impacted by hydropower exploitation and associated with large-scale mitigation stocking. Analysis was carried out by screening 82 SNPs in 1680 individuals from 13 Swedish rivers. We found an overall decrease in genetic divergence and diminished isolation by distance among populations, strongly indicating genetic homogenization over the past century. We further observed an increase in genetic diversity within populations consistent with increased gene flow. The temporal genetic change was lower in larger wild populations than in smaller wild and hatchery-reared ones, indicating that larger populations have been able to support a high number of native spawners in relation to immigrants. Our results demonstrate that stocking practices of salmon in the Baltic Sea have led to the homogenization of populations over the last century, potentially compromising their ability to adapt to environmental change. Stocking of reared fish is common worldwide, and our study is a cautionary example of the potentially long-term negative effects of such activities.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A century of genetic homogenization in Baltic salmon—evidence from archival DNA

Palm

Gilbey

Spong³

et al. 2021

Proc. R. Soc. B.

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show abstract

“…Dotted line represents equal LRS between hatchery‐ and natural‐origin fish. Due to an outlier in O'Sullivan et al ( 2020 ) (see asterisk), the Atlantic Salmon figure (a) includes an inset representing the correct scale on the y‐axis. Araki, Ardren, et al ( 2007 ) results from the traditional hatchery programs with F1 fish originating from two hatchery‐origin parents and not adjusted for angling harvest.…”

Section: The Impact Of Hatchery Origin and Captive Rearing On Lifetime Reproductive Successmentioning

confidence: 99%

An evaluation of the potential factors affecting lifetime reproductive success in salmonids

Koch

Narum

2021

Evolutionary Applications

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Lifetime reproductive success (LRS), the number of offspring produced over an organism's lifetime, is a fundamental component of Darwinian fitness. For taxa such as salmonids with multiple species of conservation concern, understanding the factors affecting LRS is critical for the development and implementation of successful conservation management practices. Here, we reviewed the published literature to synthesize factors affecting LRS in salmonids including significant effects of hatchery rearing, life history, and phenotypic variation, and behavioral and spawning interactions. Additionally, we found that LRS is affected by competitive behavior on the spawning grounds, genetic compatibility, local adaptation, and hybridization. Our review of existing literature revealed limitations of LRS studies, and we emphasize the following areas that warrant further attention in future research: (1) expanding the range of studies assessing LRS across different life‐history strategies, specifically accounting for distinct reproductive and migratory phenotypes; (2) broadening the variety of species represented in salmonid fitness studies; (3) constructing multigenerational pedigrees to track long‐term fitness effects; (4) conducting LRS studies that investigate the effects of aquatic stressors, such as anthropogenic effects, pathogens, environmental factors in both freshwater and marine environments, and assessing overall body condition, and (5) utilizing appropriate statistical approaches to determine the factors that explain the greatest variation in fitness and providing information regarding biological significance, power limitations, and potential sources of error in salmonid parentage studies. Overall, this review emphasizes that studies of LRS have profoundly advanced scientific understanding of salmonid fitness, but substantial challenges need to be overcome to assist with long‐term recovery of these keystone species in aquatic ecosystems.

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“…Across North America and Europe, implementation of captive-breeding programs is also used in combination with C&R to compensate decreasing recruitment on populations with abundance below their appropriate conservation threshold (DFO, 2008; MFFP, 2016; NASCO, 2017; ICES 2019). As for C&R, very few studies have documented patterns of reproductive success of captive-bred salmon (Milot et al 2012; O’Sullivan et al 2020). Previous research on captive-bred salmon demonstrated that minimizing time spent in captivity would alleviate unintentional domestication effect (Milot et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Captive-breeding and catch-and-release’s effects on the reproductive success of Atlantic salmon (Salmo salarL.)

Bouchard¹,

Wellband²,

Lecomte³

et al. 2021

Preprint

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Captive-breeding programs as well as and catch-and-release are among the most commonly adopted conservation practices in recreational fisheries. However, risks and benefits associated with their implementation are rarely evaluated. In the case of Atlantic Salmon, while previous studies revealed that captive-bred fish show reduced fitness compared to their wild counterparts in nature. Yet, few examined the extent and causes of their reduced reproductive success or directly compared their contribution to enhance genetic diversity to that of wild fish, including mature male parr. Furthermore, only one study specifically measured the reproductive success of caught and released Atlantic salmon in natural settings, and no study to date evaluated if released salmon are able to reproduce when released at temperature above 20°C which is known to increase post-release mortality. Here, we use high-throughput microsatellite sequencing of 38 loci to accurately assign 2500 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Quebec, Canada. The resolved molecular pedigree provided informative insight on the reproductive pattern of both captive-bred salmon and caught-and-released salmon. Captive-bred salmon had fewer partners than their wild conspecifics which lead to a significant reduction of reproductive success relative to that of their wild counterparts. Supplementation of captive-bred salmon significantly contributed to increase genetic diversity but mature male parr did so to an even greater extent and significantly inflated the number of alleles found among offspring. Moreover, our results showed that that at least 83% of caught-and-released salmon did successfully reproduced although caught-and-released female salmon have a significantly reduced reproductive success, averaging 73% of the reproductive output of non-caught salmon. Reproductive success of released salmon was not influenced by water temperature over 20°C which suggests either that the studied population is locally adapted to warm waters or that they behaviorally regulated body temperature by accessing nearby thermal refugia. Our results should help refining managers' ability to analyze the risks and benefits associated with captive-breeding and catch-and-release, and thus, optimize conservation practices used for the preservation of Atlantic salmon populations.

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Captive-bred Atlantic salmon released into the wild have fewer offspring than wild-bred fish and decrease population productivity

Cited by 41 publications

References 56 publications

A century of genetic homogenization in Baltic salmon—evidence from archival DNA

A century of genetic homogenization in Baltic salmon—evidence from archival DNA

An evaluation of the potential factors affecting lifetime reproductive success in salmonids

Captive-breeding and catch-and-release’s effects on the reproductive success of Atlantic salmon (Salmo salarL.)

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