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43555: 200305400 EXP REPRO OF STEELHEAD IN HOOD RIVER 2010
54599: 2003-054-00 EXP REPRO OF STEELHEAD IN HOOD RIVER
Contract Status:
Closed
Contract Description:
PROJECT COORDINATION AND PARTNERSHIPS
The genetics pedigree work will be carried out by Michael Blouin at Oregon State University. This project is coordinated with the Hood River steelhead hatchery and research program, funded by Bonneville Power Administration and administered and implemented by the Oregon Department of Fish and Wildlife and the Warm Springs Tribes (project numbers 198805307, 198805308, 198805304 and 198805303). These projects include operation and maintenance of the Oak Springs and Parkdale hatchery facilities, and operation and maintenance of the fish collection and handling facility at Powerdale Dam, as well as database management and data analysis on the part of ODFW. We will also collaborate with Jeri Bartholomew at OSU and the salmon disease lab.
LOCATION OF PROJECT
Steelhead samples were collected at Powerdale Dam, Hood River, under supervision of Rod French, ODFW, who will also ... coordinate aging of scale samples. Crosses of fish for experiments are carried out by staff at the Parkdale Hatchery, and families are raised at Oak Springs hatchery. All laboratory work and genetics data analysis to be conducted in the laboratory of Michael Blouin at Oregon State University.
BACKGROUND AND RESULTS TO DATE FROM THE HOOD RIVER
The Hood River supports two populations of steelhead, a summer run and a winter run. They spawn only above the Powerdale Dam, which is a complete barrier to all salmonids. Since 1991 every adult passed above the dam has been measured, cataloged and sampled for scales or fin snip. Therefore, we have a DNA sample from every adult steelhead that went over the dam to potentially spawn in the Hood River from 1991 to the present. Similar numbers of hatchery and wild fish have been passed above the dam during the last decade. During the 1990's "old" domesticated hatchery stocks of each run (multiple generations in the hatchery, out-of-basin origin; hereafter “Hold”) were phased out, and conservation hatchery programs were started for the purpose of supplementing the two wild populations (hereafter "new" hatchery stocks, “Hnew”). The winter-run Hnew were started in 1991, and the summer-run Hnew were started in 1997. In a supplementation program such as this, wild-born broodstock are used as parents in the hatchery in an attempt to circumvent the low fitness induced by multiple generations of selection in the hatchery. These samples give us the unprecedented ability to estimate, via microsatellite-based pedigree analysis, the relative total reproductive success (adult to adult production) of hatchery (H) and wild (W) fish for two populations (summer and winter), over multiple brood years. We now have a three-generation pedigree that is complete for all anadromous fish. Note, however, that we are missing samples from resident fish that apparently are the parents of many steelhead. We compared the relative success of two "old" hatchery stocks vs. wild fish (the winter run “Big Creek” stock and the summer run “Skamania” stock), and showed they have much lower total fitness than wild fish when both breed in the wild (Araki et al., 2007a). In that paper we also concluded that the winter-run Hnew were not significantly different from wild fish, based on 3 run years of data. But in a subsequent analysis based on six run years of data the difference was significant, with the Hnew winter run fish averaging about 85% the fitness of wild fish (Araki et al., 2007d).
One problem with interpreting an observed difference in fitness between fish raised in a hatchery and fish raised in the wild is that the difference can have a genetic and/or environmental basis (because the H fish experienced a very different environment during the juvenile phase). Therefore, the question of whether the hatchery effect is genetic or environmental in origin is very important. In Araki et al. (2007d) we were also able to compare the first generation, Hnew fish with second-generation hatchery fish raised in the same hatchery. These data suggest that the second generation fish have ~55% the reproductive fitness of the first generation fish (Araki et al., 2007d). Because both types of fish experienced identical environments, the difference between them must be genetically based. This result also suggests that the decline in fitness that results from recycling “hatchery genes” back through the hatchery can occur very quickly.
Thus, we have demonstrated a genetically-based effect of hatchery culture that reduces fitness in the wild and that accumulates with each generation of hatchery culture. Nevertheless, even if captive-bred individuals are genetically different and produce fewer offspring than wild individuals, adding them to a wild population can still give a demographic boost without substantial harm to a wild population that is below carrying capacity if (1) the genetic effects do not persist into the next generation (i.e., natural selection purges the offspring generation of their deleterious alleles before they reproduce), and (2) enough captive-bred individuals are added each generation to make up for their lower productivity. If the first condition is not true, however, genetic effects will accumulate over time, potentially leading to a downward spiral in the absolute fitness of the supplemented wild population. Thus, the key question is whether the wild-born descendents of captive-bred fish are less reproductively successful than the descendents of wild fish. With the completion of the third generation of the pedigree (i.e. figure 1 in Araki et al., 2009) we have now been able to analyze the fitness of wild-born fish as a function of their parentage. We found that wild-born offspring of two first-generation hatchery fish averaged 37% the fitness of the offspring of wild fish, while offspring of hatchery-by-wild crosses averaged 87% (Araki et al., 2009). These results suggest that the hatchery genetic load is not purged from the wild-born population after a full generation of natural selection in the wild.
To summarize the work to date on the Hood River, we have shown: (1) the older, multi-generation, summer and winter hatchery stocks from the Hood River had very low fitness relative to wild fish (10-30%). This result is consistent with results of many other studies on old stocks (Berejikian and Ford, 2004; Araki et al., 2008). (2) first generation winter run fish have significantly lower fitness than wild fish (about 85%), second generation fish do even worse, and the effect is genetically based. (3) The genetic effects of hatchery culture identified for the winter-run stock persist into the first wild-born generation, with the fitness of wild-born fish depending on whether their parents were both wild, both hatchery or one of each. Again, the common environment experienced by these three types of wild fish suggests a genetic effect.
In addition to completing our main mission of analyzing the fitness of hatchery and wild fish and their descendents, we have also addressed several other applied and basic questions. These topics include the effects of hatchery stock and resident fish on the effective size of the Hood River population (Araki et al., 2007b) and methodological work on methods for fitness estimation (Araki and Blouin, 2005) and estimation of effective size (Araki et al., 2007c). We just finished testing what fraction of missing parents were hatchery residualized fish, and found that only a very few could have been. Therefore, residualized hatchery fish are not a significant route of gene flow from the hatchery into the wild steelhead population. We are also in the process of analyzing the fitness of repeat spawners versus that of fish that spawn only once.
CONTINUING AND FUTURE WORK
We will focus on the following three questions (see the Narrative of Work Element C (162) ‘Analyze/Interpret data’ for additional background and references):
(1) How general are the results that we found for winter-run steelhead in the Hood River?
It was no surprise that older stocks had extremely low fitness, but the low fitness of the first and second generation winter-run hatchery fish was unexpected. Because of the management implications of our results, it is important to assess their generality. We can now estimate the relative fitness of the first-generation hatchery summer-run steelhead in the Hood River. Because the winter and summer run are reproductively independent and breed in different forks of the Hood River, these summer-run data will represent an independent test of the hypothesis that first-generation hatchery steelhead have lower fitness than wild fish.
(2) What are the mechanisms that cause the rapid decline?
This is probably the most important question that needs to be answered. It appears that strong selection in some part of the life cycle is causing hatchery fish to quickly evolve to be different than wild fish. But we do not know which traits are involved. The answer to this question would help identify ways to modify the hatchery experience in order to lessen those selection pressures. Here we will test the hypothesis that the hatchery is inadvertently selecting for juveniles that have an unusually fast growth rate. We will also test whether having a hatchery background also makes fish more susceptible to diseases, as would be expected given the usual tradeoff between allocations of energy to growth versus other life history traits such a maintenance (disease resistance) and reproduction.
REFERENCES CITED
Araki, H. and M.S. Blouin. 2005. Unbiased estimation of relative reproductive success of different groups: evaluation and correction of bias caused by parentage assignment errors. Molecular Ecology, 13:4907-4110.
Araki, H., W.R. Ardren, E. Olsen, B. Cooper and M.S. Blouin. 2007a. Reproductive success of captive-bred steelhead trout in the wild: evaluation of three hatchery programs in the Hood River. Conservation Biology 21:181-190.
Araki, H., R.S. Waples, W.R. Ardren, B. Cooper and M.S. Blouin. 2007b. Effective population size of steelhead trout: influence of variance in reproductive success, hatchery programs, and genetic compensation between life-history forms. Molecular Ecology 16:953-966
Araki, H., R.S. Waples and M.S. Blouin. 2007c. A potential bias in the temporal method for estimating Ne in admixed populations under natural selection. Molecular Ecology 16: 2261–2271
Araki, H., B. Cooper and M.S. Blouin. 2007d. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318: 100-103.
Araki, H., B. Berejikian, M. Ford, and M.S. Blouin. 2008 Fitness of hatchery-reared salmonids in the wild. Evolutionary Applications 1:342-355.
Araki, H., B. Cooper and M.S. Blouin. 2009. Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendents n the wild. Biology Letters doi: 10.1098/rsbl.2009.0315
Berejikian, B. A., and M. J. Ford. 2004. Review of the Relative Fitness of Hatchery and Natural Salmon. U.S. Dept. Commer., NOAA Tech. Memo. NMFS-NWFSC-61. 28 p. Northwest Fisheries Science Center, Seattle, WA.
Account Type(s):
Expense
Contract Start Date:
10/01/2010
Contract End Date:
09/30/2011
Current Contract Value:
$291,023
Expenditures:
$291,023
* Expenditures data includes accruals and are based on data through 31-Mar-2025.
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The Contractor shall report on the status of milestones and deliverables in Pisces. Reports shall be completed either monthly or quarterly as determined by the BPA COTR. Additionally, when indicating a deliverable milestone as COMPLETE, the contractor shall provide metrics and the final location (latitude and longitude) prior to submitting the report to the BPA COTR.
Categorical Exclusion Applied (from Subpart D, 10 C.F.R. Part 1021): B3.3: Field and laboratory research, inventory, and information collection activities that are directly related to the conservation of fish or wildlife resources and that involve only negligible habitat destruction or population reduction.
Summarize statistics for fish genotyped to date, give progress assessment. Approximately 750 new fish genotyped by end of each reporting quarter. More details on loci and methods are explained in Araki et al., (2006; Conservation Biology, 21:181-190).
Our data analysis efforts over the next year will focus on the following three actions:
(1) Estimate fitness of summer-run Hnew fish relative to that of wild summer-run
It is important to know whether our results with the winter-run steelhead are a special case, or are typical of hatchery supplementation programs. Several other research groups are in the process of examining the relative fitness of first-generation hatchery salmon of various species (coho, Chinook, steelhead), so eventually we will have a basis for comparison. But these studies have not published their results yet. We can now analyze the relative fitness of the first-generation summer-run steelhead stock that were released into the Hood River beginning in 1997. Those hatchery fish began returning in appreciable numbers in 2000. Because the winter and summer run are reproductively independent and breed in different parts of the Hood River, these summer-run data should constitute an independent test of the hypothesis that first-generation hatchery steelhead have lower fitness than wild fish. As part of the FY 2010 objectives we have been analyzing the first two run years (2000 and 2001) in which these summer-run Hnew bred in the wild (for these two years we should now have in hand >95% of their returning offspring). We will continue with the next year, with the ultimate goal of having four years of comparisons between Hnew summers and wild fish.
(2) Test whether offspring of hatchery fish grow faster under hatchery conditions than the offspring of wild fish
The 30-40% per generation drop in fitness that we estimated is occurring per hatchery generation in the winter run (Araki et al., 2007d) is so extreme that it was questionable whether domestication selection was even a plausible explanation. Here “domestication selection” means both positive selection for traits that are favored in the hatchery and relaxation of natural selection. We did a quantitative genetic analysis of selection in alternating environments and showed that strong selection was indeed a sufficient explanation for our results (Araki et al., 2008). So now the question becomes, what traits are involved?
Both adult traits and juvenile traits could be the targets of positive selection or relaxed natural selection. Artificial spawning in the hatchery almost certainly results in relaxation of mate selection (Berejikian et al.2000; de Gaudemar et al. 2000), intra-sexual competition, and selection on traits such as body size, egg size, fecundity and spawn timing and location (van den Bergheand Gross 1989; Fleming and Gross 1994; Einum and Fleming 2000). As for juvenile traits, given only 5-15% mortality in hatcheries, there is not enough selective death to generate the fitness declines observed. So the effect cannot be explained simply by viability (survival) selection on some trait in the hatchery. On the other hand, mortality from smolt to adult is often > 99%. So juvenile traits that affect adult survival (or perhaps even breeding behaviors) could well be the targets of selection. For example, smolt size is positively correlated with ocean survival, so there is strong selection on size at release (Reisenbichler et al., 2004). In the high-food and predator-free hatchery environment, this survival difference should select for high growth rate in hatchery juveniles, perhaps via behavioral or metabolic changes. But an excessively high growth rate can be maladaptive in natural environments (Arendt, 1997). So when those surviving hatchery fish reproduce in a natural setting, their offspring could have lower survival than wild offspring owing to inappropriate behaviors, an excessively high metabolism, or other maladaptive consequences of a genetic predisposition for fast growth in the benign and high-food hatchery environment (Sundstrom et al., 2005; Biro et al., 2004; Tymchuk et al., 2007). Therefore, we have begun testing whether there is evidence that the Hood River hatchery fish have been selected to have higher growth rates under hatchery conditions. In 2008 we set up a series of 2x2 matrix crosses involving a hatchery and wild male by a hatchery and wild female, and then raised each pooled group of four families in the hatchery for seven weeks. We measured the size of each fish and archived a tissue sample for DNA typing. After sorting them back into their respective families, we found no evidence for an additive genetic effect of hatchery versus wild background, although there was a weak maternal effect in which the offspring of wild females seemed to grow faster (perhaps an effect of egg size?). We started a second set of crosses in 2009 and sampled them at 2 months of age and one year of age. Among the 2-month olds we again found little evidence for a difference between fish of H vs. W backgrounds. We now have their siblings raised to one year of age, and plan to analyze them the same way. It is possible that any growth difference will appear later in life, so we haven’t rule out the growth rate hypothesis yet. Finally, we are setting up a 3rd set of crosses this summer, and will replicate the experiment in one final year, although raising them at densities that more closely match those of the production fish (last year’s fish were not as crowded). If we still see no effect of genetic background, then we will consider the growth rate hypothesis to be not so compelling.
(3) Test of differential disease resistance:
In collaboration with Jeri Bartholomew at OSU, we will attempt to test the siblings of this year’s crosses with viral and bacterial challenges. These experiments are to be conducted at the salmon disease lab at OSU. The fish will be challenged in groups and we will sort them back into their respective families after the fact via microsatellites, as with the growth rate study. Our hypothesis is that fish of H background will be less disease resistant as a consequence of hatchery selection for growth (i.e. selection to invest energetic resources into growth at the expense of maintenance). We haven't done this before, so we aren't guaranteeing that this first year's experiment will work (e.g. we have to estimate the proper challenge doses, fish can die for other reasons, and so on). But if it does work, and we do find a difference, it will be a very interesting corroborating evidence for selection on key life history traits as the mechanism of domestication.
References cited:
Araki, H., W.R. Ardren, E. Olsen, B. Cooper and M.S. Blouin. 2007a. Reproductive success of captive-bred steelhead trout in the wild: evaluation of three hatchery programs in the Hood River. Conservation Biology 21:181-190.
Araki, H., B. Cooper and M.S. Blouin. 2007d. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318: 100-103.
Araki, H., B. Berejikian, M. Ford, and M.S. Blouin. 2008 Fitness of hatchery-reared salmonids in the wild. Evolutionary Applications 1:342-355.
Arendt, J.D.. 1997. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 72:149-177.
Berejikian, B. A., E. P. Tezak, and A. L. LaRae. 2000. Female mate choice and spawning behavior of chinook salmon under experimental conditions. Journal of Fish Biology 57:647–661.
van den Berghe, E. P., and M. R. Gross. 1989. Natural selection resulting from female breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch). Evolution 43:125–140
Biro, P. A., M. V. Abrahams, J. R. Post, and E. A. Parkinson. 2004. Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proceedings: Biological Sciences 271:2233.
Einum, S., and I. A. Fleming. 2000. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639.
Fleming, I. A., and M. R. Gross. 1994. Breeding success of hatchery and wild coho salmon (Oncorhynchus kisutch) in competition. Ecological Applications 3:230–245.
de Gaudemar, B., J. M. Bonzom, and E. Beall. 2000. Effects of courtship and relative mate size on sexual motivation in Atlantic salmon. Journal of Fish Biology 57:502–515.
Reisenbichler, R., S. Rubin, L. Wetzel, and S. Phelps. 2004. Natural selection after release from a hatchery leads to domestication in steelhead, Oncorhynchus mykiss. Pp. 371-383 in B. R. Howell, E. Moksness and T. Svåsand, eds. Stock enhancement and sea ranching. Oxford, Malden, MA.
Seamons, T. R., P. Bentzen, and T. P. Quinn. 2004. The mating system of steelhead, Oncorhynchus mykiss, inferred by molecular analysis of parents and progeny. Environmental Biology of Fishes 69: 333–344
Sundstrom, L. F., M. Lohmus, R. H. Devlin, and E. Brainerd. 2005. Selection On Increased Intrinsic Growth Rates In Coho Salmon, Oncorhynchus Kisutch. Evolution 59:1560.
Tymchuk, W. E., L. F. Sundstrom, and R. H. Devlin. 2007. Growth And Survival Trade-Offs And Outbreeding Depression In Rainbow Trout (Oncorhynchus Mykiss). Evolution 61:1225.
.Zimmerman, C. E., and G. H. Reeves. 2000. Population structure of sympatric anadromous and nonanadromous Oncorhynchusmykiss: evidence from spawning surveys and otolith microchemistry. Canadian Journal of Fisheries and Aquatic Sciences 57:2152–2162
Post doc and/or principal investigator to attend at least one national or international scientific meeting for purpose of presenting current data and discussing work with colleagues. Meetings are usually in the summer months. It is important that the post doc and/or principal investigator meet regularly with colleagues who are doing similar work, and that we keep the scientific community informed about our latest results. This year we plan to attend at least one national or international meeting to to present our year-to-date results on the fitness of each type of fish.
Administrative work in support of on the ground efforts and in support of BPA's programmatic requirements such as metric reporting, financial reporting (e.g. accruals), and development of SOW package (includes draft and final SOW, budget and property inventory).
Submit Annual Report for October 2009 to September 2010
The progress report summarizes FY11 tasks and results. goals, objectives, hypotheses, completed and uncompleted deliverables, problems encountered, lessons learned, and long-term planning.
Activities documented in submitted annual report and manuscripts.
Progress reports must conform to BPA guidelines. See the "formatting guidelines" link at the Technical Reports and Publications page: https://www.cbfish.org/Help.mvc/GuidanceDocuments.
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