Temporal Dynamics of DNA Methylation Patterns in Response to Rearing Juvenile Steelhead (Oncorhynchus mykiss) in a Hatchery versus Simulated Stream Environment.

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.

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

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.

Dimethylsulfoniopropionate (DMSP) Increases Survival of Larval Sablefish, Anoplopoma fimbria.

High concentrations of dimethylsulfoniopropionate (DMSP), a chemical compound released by lysed phytoplankton, may indicate high rates of grazing by zooplankton and may thus be a foraging cue for planktivorous fishes. Previous studies have shown that some planktivorous fishes and birds aggregate or alter locomotory behavior in response to this chemical cue, which is likely adaptive because it helps them locate prey. These behavioral responses have been demonstrated in juveniles and adults, but no studies have tested for effects on larval fish. Larvae suffer from high mortality rates and are vulnerable to starvation. While larvae are generally thought to be visual predators, they actually have poor vision and cryptic prey. Thus, larval fish should benefit from a chemical cue that provides information on prey abundance. We reared larval sablefish, Anoplopoma fimbria, for one week and supplemented feedings with varying concentrations of DMSP to test the hypothesis that DMSP affects larval survival. Ecologically relevant DMSP concentrations increased larval survival by up to 70 %, which has implications for production in aquaculture and recruitment in nature. These results provide a new tool for increasing larval production in aquaculture and also suggest that larvae may use DMSP as an olfactory cue. The release of DMSP may be a previously unappreciated mechanism through which phytoplankton affect larval survival and recruitment.

Gene flow between sympatric life history forms of Oncorhynchus mykiss located above and below migratory barriers.

Oncorhynchus mykiss have a diverse array of life history types, and understanding the relationship among types is important for management of the species. Patterns of gene flow between sympatric freshwater resident O. mykiss, commonly known as rainbow trout, and anadromous O. mykiss, commonly known as steelhead, populations are complex and poorly understood. In this study, we attempt to determine the occurrence and pathways of gene flow and the degree of genetic similarity between sympatric resident and anadromous O. mykiss in three river systems, and investigate whether resident O. mykiss are producing anadromous offspring in these rivers, two of which have complete barriers to upstream migration. We found that the population structure of the O. mykiss in these rivers appears to be influenced more by the presence of a barrier to upstream migration than by life history type. The sex ratio of resident O. mykiss located above a barrier, and smolts captured in screw traps was significantly skewed in favor of females, whereas the reverse was true below the barriers, suggesting that male resident O. mykiss readily migrate downstream over the barrier, and that precocious male maturation may be occurring in the anadromous populations. Through paternity analyses, we also provide direct confirmation that resident O. mykiss can produce offspring that become anadromous. Most (89%) of the resident O. mykiss that produced anadromous offspring were males. Our results add to the growing body of evidence that shows that gene flow does readily occur between sympatric resident and anadromous O. mykiss life history types, and indicates that resident O. mykiss populations may be a potential repository of genes for the anadromous life history type.

A floating bridge disrupts seaward migration and increases mortality of steelhead smolts in Hood Canal, Washington state.

BACKGROUND: Habitat modifications resulting from human transportation and power-generation infrastructure (e.g., roads, dams, bridges) can impede movement and alter natural migration patterns of aquatic animal populations, which may negatively affect survival and population viability. Full or partial barriers are especially problematic for migratory species whose life histories hinge on habitat connectivity. METHODOLOGY/PRINCIPAL FINDINGS: The Hood Canal Bridge, a floating structure spanning the northern outlet of Hood Canal in Puget Sound, Washington, extends 3.6 meters underwater and forms a partial barrier for steelhead migrating from Hood Canal to the Pacific Ocean. We used acoustic telemetry to monitor migration behavior and mortality of steelhead smolts passing four receiver arrays and several single receivers within the Hood Canal, Puget Sound, and Strait of Juan de Fuca. Twenty-seven mortality events were detected within the vicinity of the Hood Canal Bridge, while only one mortality was recorded on the other 325 receivers deployed throughout the study area. Migrating steelhead smolts were detected at the Hood Canal Bridge array with greater frequency, on more receivers, and for longer durations than smolts migrating past three comparably configured arrays. Longer migration times and paths are likely to result in a higher density of smolts near the bridge in relation to other sites along the migration route, possibly inducing an aggregative predator response to steelhead smolts. CONCLUSIONS/SIGNIFICANCE: This study provides strong evidence of substantial migration interference and increased mortality risk associated with the Hood Canal Bridge, and may partially explain low early marine survival rates observed in Hood Canal steelhead populations. Understanding where habitat modifications indirectly increase predation pressures on threatened populations helps inform potential approaches to mitigation.

Variation in the early marine survival and behavior of natural and hatchery-reared Hood Canal steelhead.

BACKGROUND: Hatchery-induced selection and direct effects of the culture environment can both cause captively bred fish populations to survive at low rates and behave unnaturally in the wild. New approaches to fish rearing in conservation hatcheries seek to reduce hatchery-induced selection, maintain genetic resources, and improve the survival of released fish. METHODOLOGY/PRINCIPAL FINDINGS: This study used acoustic telemetry to compare three years of early marine survival estimates for two wild steelhead populations to survival of two populations raised at two different conservation hatcheries located within the Hood Canal watershed. Steelhead smolts from one conservation hatchery survived with probabilities similar to the two wild populations (freshwater: 95.8-96.9%, early marine: 10.0-15.9%), while smolts from the other conservation hatchery exhibited reduced freshwater and early marine survival (freshwater: 50.2-58.7%, early marine: 2.6-5.1%). Freshwater and marine travel rates did not differ significantly between wild and hatchery individuals from the same stock, though hatchery smolts did display reduced migration ranges within Hood Canal. Between-hatchery differences in rearing density and vessel geometry likely affected survival and behavior after release and contributed to greater variation between hatcheries than between wild populations. CONCLUSIONS/SIGNIFICANCE: Our results suggest that hatchery-reared smolts can achieve early marine survival rates similar to wild smolt survival rates, and that migration performance of hatchery-reared steelhead can vary substantially depending on the environmental conditions and practices employed during captivity.

Early marine migration patterns of wild coastal cutthroat trout (Oncorhynchus clarki clarki), steelhead trout (Oncorhynchus mykiss), and their hybrids.

BACKGROUND: Hybridization between coastal cutthroat trout (Oncorhynchus clarki clarki) and steelhead or rainbow trout (Oncorhynchus mykiss) has been documented in several streams along the North American west coast. The two species occupy similar freshwater habitats but the anadromous forms differ greatly in the duration of marine residence and migration patterns at sea. Intermediate morphological, physiological, and performance traits have been reported for hybrids but little information has been published comparing the behavior of hybrids to the pure species. METHODOLOGY/PRINCIPAL FINDINGS: This study used acoustic telemetry to record the movements of 52 cutthroat, 42 steelhead x cutthroat hybrids, and 89 steelhead smolts, all wild, that migrated from Big Beef Creek into Hood Canal (Puget Sound, Washington). Various spatial and temporal metrics were used to compare the behavior of the pure species to their hybrids. Median hybrid residence time, estuary time, and tortuosity values were intermediate compared to the pure species. The median total track distance was greater for hybrids than for either cutthroat or steelhead. At the end of each track, most steelhead (80%) were located near or north of the Hood Canal, as expected for this seaward migrating species, whereas most cutthroat (89%) were within 8 kilometers of the estuary. Most hybrids (70%) were detected leaving Hood Canal, though a substantial percentage (20%) remained near the Big Beef Creek estuary. More hybrids (7.5%) than pure cutthroat (4.5%) or steelhead (0.0%) were last detected in the southern reaches of Hood Canal. CONCLUSIONS/SIGNIFICANCE: Given the similarity in freshwater ecology between the species, differences in marine ecology may play an important role in maintaining species integrity in areas of sympatry.

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.