Todd R. Seamons

A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change

Salmonine fishes are commonly subjected to strong, novel selective pressures due to anthropogenic activities and global climate change, often resulting in population extinction. Consequently, there is considerable interest in predicting the long‐term evolutionary trajectories of extant populations. Knowledge of the genetic architecture of fitness traits is integral to making these predictions. We reviewed the published, peer‐reviewed literature for estimates of heritability and genetic correlation for fitness traits in salmonine fishes with two broad goals in mind: summarization of published data and testing for differences among categorical variables (e.g., species, life history type, experimental conditions). Balanced coverage of variables was lacking and estimates for wild populations and behavioral traits were nearly absent. Distributions of heritability estimates were skewed toward low values and distributions of genetic correlations toward large, positive values, suggesting that significant potential for evolution of traits exists. Furthermore, experimental conditions had a direct effect on h2 estimates, and other variables had more complex effects on h2 and rG estimates, suggesting that available estimates may be insufficient for use in models to predict evolutionary change in wild populations. Given this and other inherent complicating factors, making accurate predictions of the evolutionary trajectories of salmonine fishes will be a difficult task.

An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA

Assignment tests are increasingly applied in ecology and conservation, although empirical comparisons of methods are still rare or are restricted to few of the available approaches. Furthermore, the performance of assignment tests in cases with low population differentiation, violations of Hardy–Weinberg equilibrium and unbalanced sampling designs has not been verified. The release of adult hatchery steelhead to spawn in Forks Creek in 1996 and 1997 provided an opportunity to compare the power of different assignment methods to distinguish their offspring from those of sympatric wild steelhead. We compared standard assignment methods requiring baseline samples (frequency, distance and Bayesian) and clustering approaches with and without baseline information, using six freely available computer programs. Assignments were verified by parentage data obtained for a subset of returning offspring. All methods provided similar assignment success, despite low differentiation between wild and hatchery fish (FST = 0.02). Bayesian approaches with baseline data performed best, whereas the results of clustering methods were variable and depended on the samples included in the analysis and the availability of baseline information. Removal of a locus with null alleles and equalizing sample sizes had little effect on assignments. Our results demonstrate the robustness of most assignment tests to low differentiation and violations of assumptions, as well as their utility for ecological studies that require correct classification of different groups.

The mating system of steelhead, Oncorhynchus mykiss, inferred by molecular analysis of parents and progeny

The development of molecular markers has allowed behavioral ecologists to link parents to specific offspring, providing insights into breeding systems that were not apparent from direct observationsof the social system. Studies of this type in fishes have focused on species with male parental care such as centrarchids, and on salmonids, a family with little parental care. In order to gain further insight into the mating system of steelhead trout, Oncorhynchus mykiss, a winter-spawning species whose reproductive system is poorly known, adults returning to spawn were captured in four consecutive years in a small, unfished, wild population. Juvenile offspring were sampled by electrofishing and parentage was determined by exclusion based on a 12 locus microsatellite genotype. Both males and females mated with multiple individuals, though single pair matings were also inferred. Females and males tended to have the same number of mates (median = 1), but males were more likely to have no apparent partner (43% vs. 23% for females) and the maximum number of mates were obtained by males (range 0–10 vs. 0–5 for females). There was no difference in median arrival date by sex, but 80% of the females mated with males that had already arrived rather than males arriving with or after the females (median = 7.5, range = 1–63 days difference). Contrary to expectations, there was no evidence of size-assortative mating; larger males and larger females did not tend to mate with each other more often than would have occurred by chance. Of the juveniles with only one identified parent, most had a known mother and an unknown father rather than the reverse (88% vs. 11%). We interpret this as indirect evidence that non-anadromous males achieved a significant number of fertilizations. Thus the steelhead mating system was complex, being more strongly structured by arrival date than fish size, and including a significant genetic contribution by mature male parr.

Variation in reproductive success and effective number of breeders in a hatchery population of steelhead trout (Oncorhynchus mykiss): examination by microsatellite-based parentage analysis

Conservation programs that release captive-bred individuals into the wild to mix with naturally produced individuals are an increasingly common method of supporting or enhancing weak or reduced populations that otherwise may not be self-sustaining. Captive and supportive breeding can be important conservation tools for species with small or declining populations; however, in the case of hatcheries producing salmonid fishes, detailed evaluation of spawning programs is rare. We examined variation in reproductive success, measured by adult offspring production, from three parental generations of hatchery-bred steelhead trout (Oncorhynchus mykiss) using an exclusion-based method of genetic parentage assignment. Reproductive success varied greatly among individuals (especially males) and was correlated with fecundity and maternal spawning date. Estimates of egg to smolt survival for the population as a whole among years ranged from 64% to 95%, marine survival ranged from 0.32% to 2.30%, and the number of adults produced per female ranged from 0 to 18 and the number of adults produced per male ranged from 0 to 32. The effective number of breeders ranged from 11% to 31% of the census population size for that brood year. These ratios fell within estimates from estimates of Ne/N in chinook (O. tshawytscha) and rainbow trout (O. mykiss) hatchery populations.

Effects of Growth and Reproductive History on the Egg Size–Fecundity Trade-off in Steelhead

Abstract The allocation of energy by females into different components of reproduction is critical and includes trade-offs between egg size and number. In anadromous salmonids, it is unclear whether the allocation patterns are determined by the growing conditions experienced when the fish are in freshwater or at sea or by the females reproductive history. We collected data on length, egg size, and fecundity from female steelhead Oncorhynchus mykiss that had spent 1 year in freshwater and then 2 (designated 1.2) or 3 years at sea (1.3) before spawning for the first time. We also collected the same data from females spawning for the second time but of the same age as those spawning after 3 years for the first time (1.1S1). The older females were longer than the younger ones, but there was considerable overlap in length. The repeat-spawning fish were shorter than fish of the same age that were spawning for the first time, which reflected the reduction in growth associated with the previous spawning migratio...

Can interbreeding of wild and artificially propagated animals be prevented by using broodstock selected for a divergent life history

Two strategies have been proposed to avoid negative genetic effects of artificially propagated individuals on wild populations: (i) integration of wild and captive populations to minimize domestication selection and (ii) segregation of released individuals from the wild population to minimize interbreeding. We tested the efficacy of the strategy of segregation by divergent life history in a steelhead trout, Oncorhynchus mykiss, system, where hatchery fish were selected to spawn months earlier than the indigenous wild population. The proportion of wild ancestry smolts and adults declined by 10–20% over the three generations since the hatchery program began. Up to 80% of the naturally produced steelhead in any given year were hatchery/wild hybrids. Regression model selection analysis showed that the proportion of hatchery ancestry smolts was lower in years when stream discharge was high, suggesting a negative effect of flow on reproductive success of early‐spawning hatchery fish. Furthermore, proportions of hybrid smolts and adults were higher in years when the number of naturally spawning hatchery‐produced adults was higher. Divergent life history failed to prevent interbreeding when physical isolation was ineffective, an inadequacy that is likely to prevail in many other situations.

Relationship between effective population size, inbreeding and adult fitness‐related traits in a steelhead (Oncorhynchus mykiss) population released in the wild

Inbreeding is of concern in supportive breeding programmes in Pacific salmonids, Oncorhynchus spp, where the number of breeding adults is limited by rearing space or poor survival to adulthood, and large numbers are released to supplement wild stocks and fisheries. We reconstructed the pedigree of 6602 migratory hatchery steelhead (Oncorhynchus mykiss) over four generations, to determine the incidence and fitness consequences of inbreeding in a northwest USA programme. The hatchery maintained an effective population size, N˜e = 107.9 from F0 to F2, despite an increasing census size (N), which resulted in a decreasing Ne/N ratio (0.35 in F0 to 0.08 in F2). The reduced ratio was attributed to a small broodstock size, nonrandom transfers and high variance in reproductive success (particularly in males). We observed accumulation of inbreeding from the founder generation (in F4, percentage individuals with inbreeding coefficients Δf > 0 = 15.7%). Generalized linear mixed models showed that body length and weight decreased significantly with increasing Δf, and inbred fish returned later to spawn in a model that included father identity. However, there was no significant correlation between Δf and age at return, female fecundity or gonad weight. Similarly, there was no relationship between Δf and reproductive success of F2 and F3 individuals, which might be explained by the fact that reproductive success is partially controlled by hatchery mating protocols. This study is one of the first to show that small changes in inbreeding coefficient can affect some fitness‐related traits in a monitored population propagated and released to the wild.

Use of Parentage Assignment and DNA Genotyping to Validate Scale Analysis for Estimating Steelhead Age and Spawning History

Abstract Sound fisheries management depends on understanding life history characteristics, such as age at maturity, migration, and spawning history; hard parts, such as scales and otoliths, are commonly used to estimate values for these traits. Validation of these techniques is often difficult but critical because errors in mean values for a population can result in erroneous estimates of sustainable exploitation rates. In this study, we compared information on age and spawning history derived from genetic analysis with information from scale analysis for 1,836 individual steelhead Oncorhynchus mykiss representing two life history stages (smolt and mature adult); these fish were of hatchery and wild origin and were sampled from two rivers in Washington State over a period of 19 years. Aging error rates were less than 5% for both wild smolts and hatchery adults, but the error rate for wild adults was much higher (13%; 95% confidence interval [CI] = 1.82–29.22%). Adult scale ages were biased; scale readers ...

Stable Isotopes of Carbon and Nitrogen Indicate Differences in Marine Ecology between Wild and Hatchery-Produced Steelhead

Abstract Hatchery-produced anadromous salmonids often differ from their wild conspecifics in behavior, growth, and survival after release, but our understanding of their comparative ecology at sea is very limited. We used stable isotopes of carbon and nitrogen to test the null hypothesis that hatchery-produced steelhead Oncorhynchus mykiss from Forks Creek in southwestern Washington would be similar in trophic level and marine distribution to wild fish from the same river. Analysis of scale samples from 30 fish of each type that had migrated to sea in 2001 and 2002 (120 fish in all) revealed significant effects of year and origin on both C and N. The values for δ15N were consistent with a higher trophic level for the wild fish (mean = 10.82, SD = 0.57) than for the hatchery fish (mean = 10.51, SD = 0.59), and the δ13C values were consistent with more reliance on nearshore sources of C by wild fish (wild fish mean = −16.52, SD = 0.30; hatchery fish mean = −16.73, SD = 0.31). The wild fish showed no relatio...

Estimating the Ratio of Hatchery-Produced to Wild Adult Steelhead on the Spawning Grounds using Scale Pattern Analyses

Abstract Hatcheries produce Pacific salmon and trout Oncorhynchus spp. for many purposes, including fishery enhancement. The genetic integrity of wild populations spawning near such hatcheries may depend on the efficacy of their spatial or temporal separation from hatchery fish. We describe a simple, novel approach based on the examination of scales from an iteroparous species, steelhead O. mykiss, to evaluate whether the ratio of hatchery-produced adults to wild adults on the spawning grounds met recommended levels. In this river, migrating steelhead are diverted into the hatchery by a weir. Hatchery-produced fish are manually spawned and killed in the hatchery, whereas wild fish are passed over the weir and allowed to spawn naturally upstream from the hatchery. Therefore, in principle, all hatchery-produced adults should be captured at the hatchery on their first spawning migration. However, scales from 8.3% (58 of 699) of female and 2.6% (22 of 844) of male hatchery-produced steelhead adults showed evi...