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Increased natural reproduction and genetic diversity one generation after cessation of a steelhead trout (Oncorhynchus mykiss) conservation hatchery program.

ABSTRACT: Spatial and temporal fluctuations in productivity and abundance confound assessments of captive propagation programs aimed at recovery of Threatened and Endangered populations. We conducted a 17 year before-after-control-impact experiment to determine the effects of a captive rearing program for anadromous steelhead trout (Oncorhynchus mykiss) on a key indicator of natural spawner abundance (naturally produced nests or 'redds'). The supplemented population exhibited a significant (2.6-fold) increase in redd abundance in the generation following supplementation. Four non-supplemented (control) populations monitored over the same 17 year period exhibited stable or decreasing trends in redd abundance. Expected heterozygosity in the supplemented population increased significantly. Allelic richness increased, but to a lesser (non-significant) degree. Estimates of the effective number of breeders increased from a harmonic mean of 24.4 in the generation before supplementation to 38.9 after supplementation. Several non-conventional aspects of the captive rearing program may have contributed to the positive response in the natural population.

SUBMITTER: Berejikian BA

PROVIDER: S-EPMC5774695 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Increased natural reproduction and genetic diversity one generation after cessation of a steelhead trout (Oncorhynchus mykiss) conservation hatchery program.

Berejikian Barry A BA Van Doornik Donald M DM

PloS one 20180119 1

Spatial and temporal fluctuations in productivity and abundance confound assessments of captive propagation programs aimed at recovery of Threatened and Endangered populations. We conducted a 17 year before-after-control-impact experiment to determine the effects of a captive rearing program for anadromous steelhead trout (Oncorhynchus mykiss) on a key indicator of natural spawner abundance (naturally produced nests or 'redds'). The supplemented population exhibited a significant (2.6-fold) incr ...[more]

PMID: 29351326

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Project description:Genetic selection is often implicated as the underlying cause of heritable phenotypic differences between hatchery and wild populations of steelhead trout (Oncorhynchus mykiss) that also differ in lifetime fitness. Developmental plasticity, which can also affect fitness, may be mediated by epigenetic mechanisms such as DNA methylation. Our previous study identified significant differences in DNA methylation between adult hatchery- and natural-origin steelhead from the same population that could not be distinguished by DNA sequence variation. In the current study, we tested whether hatchery-rearing conditions can influence patterns of DNA methylation in steelhead with known genetic backgrounds, and assessed the stability of these changes over time. Eyed-embryos from 22 families of Methow River steelhead were split across traditional hatchery tanks or a simulated stream-rearing environment for 8 months, followed by a second year in a common hatchery tank environment. Family assignments were made using a genetic parentage analysis to account for relatedness among individuals. DNA methylation patterns were examined in the liver, a relatively homogeneous organ that regulates metabolic processes and somatic growth, of juveniles at two time points: after eight months of rearing in either a tank or stream environment and after a subsequent year of rearing in a common tank environment. Further, we analyzed DNA methylation in the sperm of mature 2-year-old males from the earlier described treatments to assess the potential of environmentally-induced changes to be passed to offspring. Hepatic DNA methylation changes in response to hatchery versus stream-rearing in yearling fish were substantial, but few persisted after a second year in the tank environment. However, the early rearing environment appeared to affect how fish responded to developmental and environmental signals during the second year since novel DNA methylation differences were identified in the livers of hatchery versus stream-reared fish after a year of common tank rearing. Furthermore, we found profound differences in DNA methylation due to age, irrespective of rearing treatment. This could be due to smoltification associated changes in liver physiology after the second year of rearing. Although few rearing-treatment effects were observed in the sperm methylome, strong family effects were observed. These data suggest limited potential for intergenerational changes, but highlight the importance of understanding the effects of kinship among studied individuals in order to properly analyze and interpret DNA methylation data in natural populations. Our work is the first to study family effects and temporal dynamics of DNA methylation patterns in response to hatchery-rearing.

Project description:While the goal of most conservation hatchery programs is to produce fish that are genetically and phenotypically indistinguishable from the wild stocks they aim to restore, there is considerable evidence that salmon and steelhead reared in hatcheries differ from wild fish in phenotypic traits related to fitness. Some evidence suggests that these phenotypic differences have a genetic basis (e.g., domestication selection) but another likely mechanism that remains largely unexplored is that differences between hatchery and wild populations arise as a result of environmentally-induced heritable epigenetic change. As a first step toward understanding the potential contribution of these two possible mechanisms, we describe genetic and epigenetic variation in hatchery and natural-origin adult steelhead, Oncorhynchus mykiss, from the Methow River, WA. Our main objectives were to determine if hatchery and natural-origin fish could be distinguished genetically and whether differences in epigenetic programming (DNA methylation) in somatic and germ cells could be detected between the two groups. Genetic analysis of 72 fish using 936 SNPs generated by Restriction Site Associated DNA Sequencing (RAD-Seq) did not reveal differentiation between hatchery and natural-origin fish at a population level. We performed Reduced Representation Bisulfite Sequencing (RRBS) on a subset of 10 hatchery and 10 natural-origin fish and report the first genome-wide characterization of somatic (red blood cells (RBCs)) and germ line (sperm) derived DNA methylomes in a salmonid, from which we identified considerable tissue-specific methylation. We identified 85 differentially methylated regions (DMRs) in RBCs and 108 DMRs in sperm of steelhead reared for their first year in a hatchery environment compared to those reared in the wild. This work provides support that epigenetic mechanisms may serve as a link between hatchery rearing and adult phenotype in steelhead; furthermore, DMRs identified in germ cells (sperm) highlight the potential for these changes to be passed on to future generations.

Project description:Many iteroparous fishes spawn after skipping one or more yearly cycles, which impacts recruitment estimates used for fisheries management and conservation. The physiological mechanisms underlying the development of consecutive and skip spawning life histories in fishes are not well understood. In salmonids, lipid energy reserves and/or growth are thought to regulate the initiation of reproductive maturation during a critical period ~1 year prior to spawning. The fasting spawning migration of summer-run steelhead trout (Oncorhynchus mykiss) results in significant depletion of energy reserves during the proposed critical period for repeat spawning. To determine whether and when lipid energy reserves and growth influence repeat spawning, measures of lipid energy reserves, growth rate and reproductive development were tracked in female steelhead trout from first to second spawning as a consecutive or skip spawner in captivity. Plasma triglyceride (TG) levels and growth rate were elevated by 10 weeks after spawning in reproductive (i.e. consecutive spawning) versus non-reproductive (i.e. skip spawning) individuals. Muscle lipid (ML) levels, condition factor and plasma estradiol levels increased at later time points. The early differences in plasma TG levels and increases in growth rate are attributable to differential rates of feeding and assimilation between the groups following spawning. A year after spawning, plasma TG levels, MLs and growth rate decreased in consecutive spawners, attributable to transfer of lipid reserves into the ovary. During the year prior to second spawning, energy reserves and plasma estradiol levels were higher in reproductive skip spawners versus consecutive spawners, reflecting the energy deficit after first spawning. These results suggest that the decision to initiate ovarian recrudescence occurs by 10 weeks after first spawning and are consistent with the differences in energy reserves acquired following spawning being a consequence of that decision. This information will increase the success of conservation projects reconditioning post-spawning summer-run steelhead trout.

Dataset Information

Increased natural reproduction and genetic diversity one generation after cessation of a steelhead trout (Oncorhynchus mykiss) conservation hatchery program.

Publications

Increased natural reproduction and genetic diversity one generation after cessation of a steelhead trout (Oncorhynchus mykiss) conservation hatchery program.

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