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      Phenotypic Sorting of Pink Salmon Hatchery Strays May Alleviate Adverse Impacts of Reduced Variation in Fitness‐Associated Traits

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          ABSTRACT

          Maladapted immigrants may reduce wild population productivity and resilience, depending on the degree of fitness mismatch between dispersers and locals. Thus, domesticated individuals escaping into wild populations is a key conservation concern. In Prince William Sound, Alaska, over 700 million pink salmon ( Oncorhynchus gorbuscha ) are released annually from hatcheries, providing a natural experiment to characterize the mechanisms underlying impacts to wild populations. Using a dataset of > 200,000 pink salmon sampled from 30 populations over 8 years, we detected significant body size and phenological differences between hatchery‐ and wild‐origin spawners, likely driven by competitive differences during maturation and broodstock selection practices. Variation in traits was reduced in hatchery fish, raising biodiversity concerns. However, phenotypic traits of immigrants and locals were positively correlated. We discuss possible mechanisms that may explain this pattern and how it may reduce adverse impacts associated with reduced trait variation. This study suggests that domestication impacts are likely widespread, but local adaptation may be maintained by phenotypic sorting.

          Abstract

          This study investigated phenotypic differences of hatchery‐ and natural‐origin pink salmon in Prince William Sound, Alaska. Analyzing data from over 200,000 salmon, findings indicated significant differences in body size and timing between hatchery and wild fish, with notably reduced variation in these fitness‐associated traits in hatchery fish, raising concerns about reduced biodiversity. However, a positive correlation between the traits of immigrants and locals suggests that phenotypic sorting may help maintain local adaptation despite these impacts.

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          Fitness of hatchery-reared salmonids in the wild

          Accumulating data indicate that hatchery fish have lower fitness in natural environments than wild fish. This fitness decline can occur very quickly, sometimes following only one or two generations of captive rearing. In this review, we summarize existing data on the fitness of hatchery fish in the wild, and we investigate the conditions under which rapid fitness declines can occur. The summary of studies to date suggests: nonlocal hatchery stocks consistently reproduce very poorly in the wild; hatchery stocks that use wild, local fish for captive propagation generally perform better than nonlocal stocks, but often worse than wild fish. However, the data above are from a limited number of studies and species, and more studies are needed before one can generalize further. We used a simple quantitative genetic model to evaluate whether domestication selection is a sufficient explanation for some observed rapid fitness declines. We show that if selection acts on a single trait, such rapid effects can be explained only when selection is very strong, both in captivity and in the wild, and when the heritability of the trait under selection is high. If selection acts on multiple traits throughout the life cycle, rapid fitness declines are plausible.
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            A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation.

            Here we critically review the scale and extent of adaptive genetic variation in Atlantic salmon (Salmo salar L.), an important model system in evolutionary and conservation biology that provides fundamental insights into population persistence, adaptive response and the effects of anthropogenic change. We consider the process of adaptation as the end product of natural selection, one that can best be viewed as the degree of matching between phenotype and environment. We recognise three potential sources of adaptive variation: heritable variation in phenotypic traits related to fitness, variation at the molecular level in genes influenced by selection, and variation in the way genes interact with the environment to produce phenotypes of varying plasticity. Of all phenotypic traits examined, variation in body size (or in correlated characters such as growth rates, age of seaward migration or age at sexual maturity) generally shows the highest heritability, as well as a strong effect on fitness. Thus, body size in Atlantic salmon tends to be positively correlated with freshwater and marine survival, as well as with fecundity, egg size, reproductive success, and offspring survival. By contrast, the fitness implications of variation in behavioural traits such as aggression, sheltering behaviour, or timing of migration are largely unknown. The adaptive significance of molecular variation in salmonids is also scant and largely circumstantial, despite extensive molecular screening on these species. Adaptive variation can result in local adaptations (LA) when, among other necessary conditions, populations live in patchy environments, exchange few or no migrants, and are subjected to differential selective pressures. Evidence for LA in Atlantic salmon is indirect and comes mostly from ecological correlates in fitness-related traits, the failure of many translocations, the poor performance of domesticated stocks, results of a few common-garden experiments (where different populations were raised in a common environment in an attempt to dissociate heritable from environmentally induced phenotypic variation), and the pattern of inherited resistance to some parasites and diseases. Genotype x environment interactions occurr for many fitness traits, suggesting that LA might be important. However, the scale and extent of adaptive variation remains poorly understood and probably varies, depending on habitat heterogeneity, environmental stability and the relative roles of selection and drift. As maladaptation often results from phenotype-environment mismatch, we argue that acting as if populations are not locally adapted carries a much greater risk of mismanagement than acting under the assumption for local adaptations when there are none. As such, an evolutionary approach to salmon conservation is required, aimed at maintaining the conditions necessary for natural selection to operate most efficiently and unhindered. This may require minimising alterations to native genotypes and habitats to which populations have likely become adapted, but also allowing for population size to reach or extend beyond carrying capacity to encourage competition and other sources of natural mortality.
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              Extent and scale of local adaptation in salmonid fishes: review and meta-analysis.

              What is the extent and scale of local adaptation (LA)? How quickly does LA arise? And what is its underlying molecular basis? Our review and meta-analysis on salmonid fishes estimates the frequency of LA to be ∼55-70%, with local populations having a 1.2 times average fitness advantage relative to foreign populations or to their performance in new environments. Salmonid LA is evident at a variety of spatial scales (for example, few km to>1000 km) and can manifest itself quickly (6-30 generations). As the geographic scale between populations increases, LA is generally more frequent and stronger. Yet the extent of LA in salmonids does not appear to differ from that in other assessed taxa. Moreover, the frequency with which foreign salmonid populations outperform local populations (∼23-35%) suggests that drift, gene flow and plasticity often limit or mediate LA. The relatively few studies based on candidate gene and genomewide analyses have identified footprints of selection at both small and large geographical scales, likely reflecting the specific functional properties of loci and the associated selection regimes (for example, local niche partitioning, pathogens, parasites, photoperiodicity and seasonal timing). The molecular basis of LA in salmonids is still largely unknown, but differential expression at the same few genes is implicated in the convergent evolution of certain phenotypes. Collectively, future research will benefit from an integration of classical and molecular approaches to understand: (i) species differences and how they originate, (ii) variation in adaptation across scales, life stages, population sizes and environmental gradients, and (iii) evolutionary responses to human activities.
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                Author and article information

                Contributors
                pwestley@alaska.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                08 January 2025
                January 2025
                : 15
                : 1 ( doiID: 10.1002/ece3.v15.1 )
                : e70781
                Affiliations
                [ 1 ] College of Fisheries and Ocean Sciences University of Alaska Fairbanks Fairbanks Alaska USA
                [ 2 ] Prince William Sound Science Center Cordova Alaska USA
                Author notes
                [*] [* ] Correspondence:

                Peter A. H. Westley ( pwestley@ 123456alaska.edu )

                Author information
                https://orcid.org/0000-0002-5312-140X
                https://orcid.org/0000-0002-0258-9264
                https://orcid.org/0000-0003-4190-7314
                Article
                ECE370781 ECE-2024-08-01744.R1
                10.1002/ece3.70781
                11711052
                39790723
                dc237860-5053-4260-a2ec-7eedae70765f
                © 2025 The Author(s). Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 November 2024
                : 03 September 2024
                : 27 November 2024
                Page count
                Figures: 5, Tables: 0, Pages: 13, Words: 10400
                Funding
                Funded by: Rasmuson Fisheries Research Center
                Funded by: Cooperative Institute for Climate, Ocean, and Ecosystem Studies under NOAA Cooperative Agreement, University of Washington , doi 10.13039/100021076;
                Award ID: NA20OAR4320271
                Funded by: Alvin G. Ott Fish and Wildlife Scholarship
                Funded by: Wakefield Chair Endowment
                Funded by: University of Alaska Fairbanks , doi 10.13039/100012574;
                Categories
                Behavioural Ecology
                Conservation Ecology
                Demography
                Ecological Engineering
                Genetics
                Phenology
                Population Ecology
                Spatial Ecology
                Research Article
                Research Article
                Custom metadata
                2.0
                January 2025
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.5.2 mode:remove_FC converted:08.01.2025

                Evolutionary Biology
                dispersal,hatchery–wild interactions,homing,phenology,phenotypic sorting,straying

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