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      Reduced relative fitness in hatchery‐origin Pink Salmon in two streams in Prince William Sound, Alaska

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          Abstract

          Previous studies generally report that hatchery‐origin Pacific Salmon ( Oncorhynchus spp.) have lower relative reproductive success (RRS) than their natural‐origin counterparts. We estimated the RRS of Pink Salmon ( Ogorbuscha) in Prince William Sound (PWS), Alaska using incomplete pedigrees. In contrast to other RRS studies, Pink Salmon have a short freshwater life history, freshwater habitats in PWS are largely unaltered by development, and sampling was conducted without the aid of dams or weirs resulting in incomplete sampling of spawning individuals. Pink Salmon released from large‐scale hatchery programs in PWS have interacted with wild populations for more than 15 generations. Hatchery populations were established from PWS populations but have subsequently been managed as separate broodstocks. Gene flow is primarily directional, from hatchery strays to wild populations. We used genetic‐based parentage analysis to estimate the RRS of a single generation of stray hatchery‐origin Pink Salmon in two streams, and across the odd‐ and even‐year lineages. Despite incomplete sampling, we assigned 1745 offspring to at least one parent. Reproductive success (RS), measured as sampled adult offspring that returned to their natal stream, was significantly lower for hatchery‐ vs. natural‐origin parents in both lineages, with RRS ranging from 0.03 to 0.47 for females and 0.05 to 0.86 for males. Generalized linear modeling for the even‐year lineage indicated that RRS was lower for hatchery‐origin fish, ranging from 0.42 to 0.60, after accounting for sample date (run timing), sample location within the stream, and fish length. Our results strongly suggest that hatchery‐origin strays have lower fitness in the wild. The consequences of reduced RRS on wild productivity depend on whether the mechanisms underlying reduced RRS are environmentally driven, and likely ephemeral, or genetically driven, and likely persistent across generations.

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          Rapid SNP Discovery and Genetic Mapping Using Sequenced RAD Markers

          Single nucleotide polymorphism (SNP) discovery and genotyping are essential to genetic mapping. There remains a need for a simple, inexpensive platform that allows high-density SNP discovery and genotyping in large populations. Here we describe the sequencing of restriction-site associated DNA (RAD) tags, which identified more than 13,000 SNPs, and mapped three traits in two model organisms, using less than half the capacity of one Illumina sequencing run. We demonstrated that different marker densities can be attained by choice of restriction enzyme. Furthermore, we developed a barcoding system for sample multiplexing and fine mapped the genetic basis of lateral plate armor loss in threespine stickleback by identifying recombinant breakpoints in F2 individuals. Barcoding also facilitated mapping of a second trait, a reduction of pelvic structure, by in silico re-sorting of individuals. To further demonstrate the ease of the RAD sequencing approach we identified polymorphic markers and mapped an induced mutation in Neurospora crassa. Sequencing of RAD markers is an integrated platform for SNP discovery and genotyping. This approach should be widely applicable to genetic mapping in a variety of organisms.
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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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              Genetic adaptation to captivity can occur in a single generation.

              Captive breeding programs are widely used for the conservation and restoration of threatened and endangered species. Nevertheless, captive-born individuals frequently have reduced fitness when reintroduced into the wild. The mechanism for these fitness declines has remained elusive, but hypotheses include environmental effects of captive rearing, inbreeding among close relatives, relaxed natural selection, and unintentional domestication selection (adaptation to captivity). We used a multigenerational pedigree analysis to demonstrate that domestication selection can explain the precipitous decline in fitness observed in hatchery steelhead released into the Hood River in Oregon. After returning from the ocean, wild-born and first-generation hatchery fish were used as broodstock in the hatchery, and their offspring were released into the wild as smolts. First-generation hatchery fish had nearly double the lifetime reproductive success (measured as the number of returning adult offspring) when spawned in captivity compared with wild fish spawned under identical conditions, which is a clear demonstration of adaptation to captivity. We also documented a tradeoff among the wild-born broodstock: Those with the greatest fitness in a captive environment produced offspring that performed the worst in the wild. Specifically, captive-born individuals with five (the median) or more returning siblings (i.e., offspring of successful broodstock) averaged 0.62 returning offspring in the wild, whereas captive-born individuals with less than five siblings averaged 2.05 returning offspring in the wild. These results demonstrate that a single generation in captivity can result in a substantial response to selection on traits that are beneficial in captivity but severely maladaptive in the wild.
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                Author and article information

                Contributors
                kyle.shedd@alaska.gov
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                15 March 2022
                March 2022
                : 15
                : 3 ( doiID: 10.1111/eva.v15.3 )
                : 429-446
                Affiliations
                [ 1 ] Alaska Department of Fish & Game Anchorage Alaska USA
                [ 2 ] Prince William Sound Science Center (PWSSC) Cordova Alaska USA
                Author notes
                [*] [* ] Correspondence

                Kyle R. Shedd, Alaska Department of Fish & Game, 333 Raspberry Road, Anchorage, AK 99518.

                Email: kyle.shedd@ 123456alaska.gov

                Author information
                https://orcid.org/0000-0002-0148-4241
                https://orcid.org/0000-0002-6229-568X
                https://orcid.org/0000-0002-0464-3981
                Article
                EVA13356
                10.1111/eva.13356
                8965367
                35386398
                e20aeb35-d1c3-46f7-8c92-990ed6f48b67
                © 2022 Alaska Department of Fish and Game. Evolutionary Applications 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
                : 21 January 2022
                : 03 June 2021
                : 03 February 2022
                Page count
                Figures: 7, Tables: 3, Pages: 18, Words: 14159
                Funding
                Funded by: North Pacific Research Board , doi 10.13039/100012635;
                Award ID: 1619
                Funded by: NOAA Saltonstall‐Kennedy Grant Program
                Award ID: NA16NMF4270251
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                March 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.2 mode:remove_FC converted:30.03.2022

                Evolutionary Biology
                alaska,aquaculture,fisheries,fitness,gt‐seq,hatchery,oncorhynchus,pedigree,pink salmon,population genetics,relative reproductive success,straying

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