Genotype-Temperature Interaction in the Regulation of Development,Growth, and Morphometrics in Wild-Type,and Growth-Hormone Transgenic Coho Salmon

Background

The neuroendocrine system is an important modulator of phenotype, directing cellular genetic responses to external cues such as temperature. Behavioural and physiological processes in poikilothermic organisms (e.g. most fishes), are particularly influenced by surrounding temperatures.

Methodology/Principal Findings

By comparing the development and growth of two genotypes of coho salmon (wild-type and transgenic with greatly enhanced growth hormone production) at six different temperatures, ranging between 8° and 18°C, we observed a genotype-temperature interaction and possible trend in directed neuroendocrine selection. Differences in growth patterns of the two genotypes were compared by using mathematical models, and morphometric analyses of juvenile salmon were performed to detect differences in body shape. The maximum hatching and alevin survival rates of both genotypes occurred at 12°C. At lower temperatures, eggs containing embryos with enhanced GH production hatched after a shorter incubation period than wild-type eggs, but this difference was not apparent at and above 16°C. GH transgenesis led to lower body weights at the time when the yolk sack was completely absorbed compared to the wild genotype. The growth of juvenile GH-enhanced salmon was to a greater extent stimulated by higher temperatures than the growth of the wild-type. Increased GH production significantly influenced the shape of the salmon growth curves.

Conclusions

Growth hormone overexpression by transgenesis is able to stimulate the growth of coho salmon over a wide range of temperatures. Temperature was found to affect growth rate, survival, and body morphology between GH transgenic and wild genotype coho salmon, and differential responses to temperature observed between the genotypes suggests they would experience different selective forces should they ever enter natural ecosystems. Thus, GH transgenic fish would be expected to differentially respond and adapt to shifts in environmental conditions compared with wild type, influencing their ability to survive and interact in ecosystems. Understanding these relationships would assist environmental risk assessments evaluating potential ecological effects.     

Disruption of seasonality in growth hormone-transgenic coho salmon (Oncorhynchus kisutch) and the role of cholecystokinin in seasonal feeding behavior

Seasonal variation in daily food intake is a well-documented phenomenon in many organisms including wild-type coho salmon where the appetite is noticeably reduced during periods of decreased day length and low water temperature. This reduction may in part be explained by altered production of cholecystokinin (CCK) and growth hormone (GH). CCK is a hormone produced in the brain and gut that mediates a feeling of satiety and thus has an inhibitory effect on food intake and foraging behaviour. Growth hormone (GH) enhances feeding behaviour and consequently growth, but its production is reduced during winter. The objectives of this study were: first, to compare the seasonal feeding behaviour of wild and GH-transgenic coho salmon; second, to determine the behavioural effect of blocking the action of CCK (by using devazepide) on the seasonal food intake; and third, to measure CCK expression in brain and gut tissues between the two genotypes across seasons. We found that, in contrast to wild salmon, food intake in transgenic salmon was not reduced during winter indicating that seasonal control of appetite regulation has been disrupted by constitutive production of GH in transgenic animals. Blocking of CCK increased food intake in both genotypes in all seasons. The increase was stronger in wild genotypes than transgenic fish; however blocking CCK in wild-type fish in winter did not elevate appetites to levels observed in the summer. The response to devazepide was generally faster in transgenic than in wild salmon with more rapid effects observed during summer than during winter, possibly due to a higher temperature in summer. Overall, a seasonal effect on CCK mRNA levels was observed in telencephalon with levels during winter being higher compared to the summer in wild fish, but with no seasonal effect in transgenic fish. No differences in seasonal CCK expression were found in hypothalamus. Higher levels of CCK were detected in the gut of both genotypes in winter compared to summer. Thus, CCK appears to mediate food intake among seasons in both wild-type and GH-transgenic salmon, and an altered CCK regulation may be responsible at least in part for the seasonal regulation of food intake.     

Interaction of growth hormone overexpression and nutritional status on pituitary gland clock gene expression in coho salmon,Oncorhynchus kisutch

Clock genes are involved in generating a circadian rhythm that is integrated with the metabolic state of an organism and information from the environment. Growth hormone (GH) transgenic coho salmon, Oncorhynchus kisutch, show a large increase in growth rate, but also attenuated seasonal growth modulations, modified timing of physiological transformations (e.g. smoltification) and disruptions in pituitary gene expression compared with wild-type salmon. In several fishes, circadian rhythm gene expression has been found to oscillate in the suprachiasmatic nucleus of the hypothalamus, as well as in multiple peripheral tissues, but this control system has not been examined in the pituitary gland nor has the effect of transgenic growth modification been examined. Thus, the daily expression of 10 core clock genes has been examined in pituitary glands of GH transgenic (T) and wild-type coho salmon (NT) entrained on a regular photocycle (12L: 12D) and provided either with scheduled feeding or had food withheld for 60?h. Most clock genes in both genotypes showed oscillating patterns of mRNA levels with light and dark cycles. However, T showed different amplitudes and patterns of expression compared with wild salmon, both in fed and starved conditions. The results from this study indicate that constitutive expression of GH is associated with changes in clock gene regulation, which may play a role in the disrupted behavioural and physiological phenotypes observed in growth-modified transgenic strains.     

Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch

Substantial evidence from the animal kingdom shows that there is a trade-off between benefits and costs associated with rapid somatic growth. One would therefore expect growth rates under natural conditions to be close to an evolutionary optimum. Nevertheless, natural selection in many salmonid species appears to be toward larger size and earlier emergence from spawning redds, indicating a potential for increased growth rate to evolve. We tested how selection for genetic variants (growth hormone transgenic coho salmon, Oncorhynchus kisutch, with more than doubled daily growth rate potential relative to wild genotypes) depended on predator timing and food abundance during the early period of life (fry stage). In artificial redds, fry of the fast-growing genotypes showed a highly significant developmental shift, emerging from gravel nests approximately two weeks sooner, but with an 18.6% reduced survival, relative to wild-genotype fry. In seminatural streams, fry of the fast-growing genotypes suffered higher predation than those of wild genotypes when predators were present at the time of fry emergence, but this difference was less pronounced when food was scarce. In streams where predators were introduced after emergence, fry survived equally well regardless of food availability. Surviving fry grew faster in habitats provided with more food, and fast-growing genotypes also grew faster than wild genotypes when predators arrived late and food was abundant. Fewer fish migrated downstream past a waterfall when food availability was high and in the presence of predators, and wild-genotype fry were more likely to migrate than fry of the fast-growing genotypes. After being returned to the experimental streams after migration, fast-growing genotypes survived equally well as those of the same genotypes that did not migrate, whereas migrating wild genotypes experienced higher mortality relative to those of the same genotypes that did not migrate. Comparisons of growth rates between siblings retained under hatchery conditions and those from habitats with the fastest growth in the experimental stream revealed that growth rates were similar for wild genotypes in both environments, whereas the fast-growing genotypes in the streams only realized 90% of their growth potential. The present study has shown that a major shift in developmental timing can alter critical early stages affecting survival and can have a significant effect on fitness. Furthermore, ecological conditions such as food abundance and predation pressure can strongly influence the potential for fast-growing variants to survive under natural conditions. The large-scale removal of many predatory species around the world may augment the evolution of increased intrinsic growth rates in some taxa.     

Rearing in Seawater Mesocosms Improves the Spawning Performance of Growth Hormone Transgenic and Wild-Type Coho Salmon

Growth hormone (GH) transgenes can significantly accelerate growth rates in fish and cause associated alterations to their physiology and behaviour. Concern exists regarding potential environmental risks of GH transgenic fish, should they enter natural ecosystems. In particular, whether they can reproduce and generate viable offspring under natural conditions is poorly understood. In previous studies, GH transgenic salmon grown under contained culture conditions had lower spawning behaviour and reproductive success relative to wild-type fish reared in nature. However, wild-type salmon cultured in equal conditions also had limited reproductive success. As such, whether decreased reproductive success of GH transgenic salmon is due to the action of the transgene or to secondary effects of culture (or a combination) has not been fully ascertained. Hence, salmon were reared in large (350,000 L), semi-natural, seawater tanks (termed mesocosms) designed to minimize effects of standard laboratory culture conditions, and the reproductive success of wild-type and GH transgenic coho salmon from mesocosms were compared with that of wild-type fish from nature. Mesocosm rearing partially restored spawning behaviour and success of wild-type fish relative to culture rearing, but remained lower overall than those reared in nature. GH transgenic salmon reared in the mesocosm had similar spawning behaviour and success as wild-type fish reared in the mesocosm when in full competition and without competition, but had lower success in male-only competition experiments. There was evidence of genotype×environmental interactions on spawning success, so that spawning success of transgenic fish, should they escape to natural systems in early life, cannot be predicted with low uncertainty. Under the present conditions, we found no evidence to support enhanced mating capabilities of GH transgenic coho salmon compared to wild-type salmon. However, it is clear that GH transgenic salmon are capable of successful spawning, and can reproduce with wild-type fish from natural systems.     

Alternate Directed Anthropogenic Shifts in Genotype Result in Different Ecological Outcomes in Coho Salmon Oncorhynchus kisutch Fry

Domesticated and growth hormone (GH) transgenic salmon provide an interesting model to compare effects of selected versus engineered phenotypic change on relative fitness in an ecological context. Phenotype in domestication is altered via polygenic selection of traits over multiple generations, whereas in transgenesis is altered by a single locus in one generation. These established and emerging technologies both result in elevated growth rates in culture, and are associated with similar secondary effects such as increased foraging, decreased predator avoidance, and similar endocrine and gene expression profiles. As such, there is concern regarding ecological consequences should fish that have been genetically altered escape to natural ecosystems. To determine if the type of genetic change influences fitness components associated with ecological success outside of the culture environments they were produced for, we examined growth and survival of domesticated, transgenic, and wild-type coho salmon fry under different environmental conditions. In simple conditions (i.e. culture) with unlimited food, transgenic fish had the greatest growth, while in naturalized stream tanks (limited natural food, with or without predators) domesticated fish had greatest growth and survival of the three fish groups. As such, the largest growth in culture conditions may not translate to the greatest ecological effects in natural conditions, and shifts in phenotype over multiple rather than one loci may result in greater success in a wider range of conditions. These differences may arise from very different historical opportunities of transgenic and domesticated strains to select for multiple growth pathways or counter-select against negative secondary changes arising from elevated capacity for growth, with domesticated fish potentially obtaining or retaining adaptive responses to multiple environmental conditions not yet acquired in recently generated transgenic strains.     

The glutathione antioxidant system is enhanced in growth hormone transgenic coho salmon (<Emphasis Type="Italic">Oncorhynchus kisutch</Emphasis>)

Insertion of a growth hormone (GH) transgene in coho salmon results in accelerated growth, and increased feeding and metabolic rates. Whether other physiological systems within the fish are adjusted to this accelerated growth has not been well explored. We examined the effects of a GH transgene and feeding level on the antioxidant glutathione and its associated enzymes in various tissues of coho salmon. When transgenic and control salmon were fed to satiation, transgenic fish had increased tissue glutathione, increased hepatic glutathione reductase activity, decreased hepatic activity of the glutathione synthesis enzyme γ-glutamylcysteine synthetase, and increased intestinal activity of the glutathione catabolic enzyme γ-glutamyltranspeptidase. However, these differences were mostly abolished by ration restriction and fasting, indicating that upregulation of the glutathione antioxidant system was due to accelerated growth, and not to intrinsic effects of the transgene. Increased food intake and ability to digest potential dietary glutathione, and not increased activity of glutathione synthesis enzymes, likely contributed to the higher levels of glutathione in transgenic fish. Components of the glutathione antioxidant system are likely upregulated to combat potentially higher reactive oxygen species production from increased metabolic rates in GH transgenic salmon.     

Growth hormone transgenesis does not influence territorial dominance or growth and survival of first-feeding Atlantic salmon Salmo salar in food-limited stream microcosms

This study explored the relative competitive ability and performance of first-feeding growth hormone (GH) transgenic and non-transgenic Atlantic salmon Salmo salar fry under low food conditions. Pair-wise dominance trials indicated a strong competitive advantage for residents of a contested foraging territory. Transgenic and non-transgenic individuals, however, were equally likely to be dominant. Similarly, in stream environments with limited food, the transgene did not influence the growth in mass or survival at high or low fry densities. Fry in low-density treatments, however, performed better than fry in high-density treatments. These results indicate that, under the environment examined, the growth performance of GH-transgenic and non-transgenic S. salar may be similar during first feeding, an intense period of selection in their life history. Similarities in competitive ability and growth performance with wild-type fish suggest that the capacity of transgenic S. salar to establish in natural streams may not be inhibited during early life history.     

Regulation of feeding behavior and food intake by appetite-regulating peptides in wild-type and growth hormone-transgenic coho salmon

Survival, competition, growth and reproductive success in fishes are highly dependent on food intake, food availability and feeding behavior and are all influenced by a complex set of metabolic and neuroendocrine mechanisms. Overexpression of growth hormone (GH) in transgenic fish can result in greatly enhanced growth rates, feed conversion, feeding motivation and food intake. The objectives of this study were to compare seasonal feeding behavior of non-transgenic wild-type (NT) and GH-transgenic (T) coho salmon (Oncorhynchus kisutch), and to examine the effects of intraperitoneal injections of the appetite-regulating peptides cholecystokinin (CCK-8), bombesin (BBS), glucagon-like peptide-1 (GLP-1), and alpha-melanocyte-stimulating hormone (α-MSH) on feeding behavior. T salmon fed consistently across all seasons, whereas NT dramatically reduced their food intake in winter, indicating the seasonal regulation of appetite can be altered by overexpression of GH in T fish. Intraperitoneal injections of CCK-8 and BBS caused a significant and rapid decrease in food intake for both genotypes. Treatment with either GLP-1 or α-MSH resulted in a significant suppression of food intake for NT but had no effect in T coho salmon. The differential response of T and NT fish to α-MSH is consistent with the melanocortin-4 receptor system being a significant pathway by which GH acts to stimulate appetite. Taken together, these results suggest that chronically increased levels of GH alter feeding regulatory pathways to different extents for individual peptides, and that altered feeding behavior in transgenic coho salmon may arise, in part, from changes in sensitivity to peripheral appetite-regulating signals.     

Oxygen uptake of growth hormone transgenic coho salmon during starvation and feeding

Oxygen uptake of growth hormone transgenic coho salmon Oncorhynchus kisutch was measured in individual fish with a closed-system respirometer and was compared with that of similar-sized non-transgenic control coho salmon during starvation and when fed a fixed ration or to satiation. Transgenic and control fish did not differ in their standard oxygen uptake after 4 days of starvation, although control fish had a higher routine oxygen uptake, scope for spontaneous activity and initial acclimation oxygen uptake. During feeding, transgenic fish ate significantly more than control fish, and had an overall oxygen uptake that was 1·7 times greater than control fish. When fish that had eaten the same per cent body mass were compared, transgenic fish had an oxygen uptake that was 1·4 times greater than control fish. Differences in oxygen uptake in growth hormone transgenic coho salmon and non-transgenic fish appear to be due to the effects of feeding, acclimation and activity level, and not to a difference in basal metabolism.     

Effects of species, culture history, size and residency on relative competitive ability of salmonids

The relative competitive ability of juvenile farm and wild salmonids was investigated to provide insight into the potential effects of introduction of cultured salmon on wild Pacific salmonid ( Oncorhynchus ) species. Aquarium experiments involving equal contests ( i.e. size matched, simultaneously introduced individuals) indicated that two wild coho salmon Oncorhynchus kisutch populations were competitively equal to a farm coho salmon population. In equal contests between farm Atlantic salmon Salmo salar (Mowi strain) and these wild coho salmon populations or coastal cutthroat trout Oncorhynchus clarki clarki , Atlantic salmon were subordinate in all cases. When Atlantic salmon were given a residence advantage, however, they were competitively equal to both wild coho salmon populations, but remained subordinate to coastal cutthroat trout. When Atlantic salmon were given a 10–30% length advantage, they were competitively equal to one wild coho salmon population but remained subordinate to the other. In equal contests in semi-natural stream channels, both wild coho and farm Atlantic salmon grew significantly more in the presence of the other species than when alone. It appears that coho salmon obtain additional food ration by out competing Atlantic salmon, whereas Atlantic salmon were stimulated to feed more in the presence of coho salmon competitors. These results suggest that wild coho salmon and cutthroat trout should out compete farm Atlantic salmon of a similar size in nature. As the relative competitive ability of Atlantic salmon improves when they have a size and residence advantage, should feral populations become established, they may exist on a more equal competitive footing owing to the long freshwater residence of Atlantic salmon.     

Disease resistance and health parameters of growth-hormone transgenic and wild-type coho salmon,Oncorhynchus kisutch

To extend previous findings regarding fish health and disease susceptibility of growth-enhanced fish, hematological and immunological parameters have been compared between growth hormone (GH) transgenic and wild-type non-transgenic coho salmon (Oncorhynchus kisutch). Compared to non-transgenic coho salmon, transgenic fish had significantly higher hematocrit (Hct), hemoglobin (Hb), mean cellular hemoglobin (MCH), mean cellular volume (MCV), and erythrocyte numbers, and lower white cell numbers. In addition, resistance to the bacterial pathogen Aeromonas salmonicida (causal agent of furunculosis) has been assessed between the strains. Higher susceptibility of transgenic fish to this disease challenge was observed in two separate year classes of fish. The present findings provide fundamental knowledge of the disease resistance on GH enhanced transgenic coho salmon, which is of importance for assessing the fitness of transgenic strains for environmental risk assessments, and for improving our understanding effects of growth modification on basic immune functions.     

Genetically enhanced growth causes increased mortality in hypoxic environments

Rapid growth and development are associated with several fitness-related benefits. Yet, organisms usually grow more slowly than their physiological maximum, suggesting that rapid growth may carry costs. Here we use coho salmon (Oncorhynchus kisutch) eggs of wild and transgenic genotypes to test whether rapid growth causes reduced tolerance to low levels of oxygen (hypoxia). Eggs were exposed to four different durations of hypoxia, and survival and growth were recorded until the end of the larval stage. Survival rates decreased with increasing duration of hypoxia, but this decrease was most pronounced for the transgenic group. Larval mass was also negatively affected by hypoxia; however, transgenic genotypes were significantly larger than wild genotypes at the end of the larval stage. Oxygen can be a limiting factor for survival and development in a wide range of organisms, particularly during the egg stage. Thus, the reduced ability of fast-growing genotypes to cope with low oxygen levels identified in the present study may represent a general constraint on evolution of rapid growth across taxa.     

Effects of food ration on SMR: influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch)

1. Consistency of differences in standard metabolic rate (SMR) between individual juvenile salmonids and the apparently limited ability of individuals to regulate their SMR has led many researchers to conclude that differences in individual SMR are fixed (i.e. genetic). 2. To test for the effects of food ration on individual performance and metabolism, SMR was estimated by measuring oxygen consumption using flow-through respirometry on individually separated young of the year coho salmon (Oncorhynchus kisutch) placed on varying food rations over a period of 44 days. 3. Results demonstrate that the quantity of food consumed directly affects SMR of juvenile coho salmon, independent of specific dynamic action (SDA, an elevation in metabolic rate from the increased energy demands associated with digestion immediately following a meal) and indicates that higher food consumption is a cause of elevated SMR rather than a consequence of it. Juvenile coho salmon therefore demonstrated an ability to regulate their SMR according to food availability and ultimately food consumption. 4. This study indicates that food consumption may play a pivotal role in understanding individual variation in SMR independent of inherent genetic differences. We suggest that studies involving SMR need to be cautious about the effects of intra-individual differences in food consumption in communal tanks or in different microhabitats in the wild as disproportionate food consumption may contribute more to variation in SMR than intrinsic (genetic) factors. 5. In general, our results suggest that evolutionary changes in SMR are likely a response to selection on food consumption and growth, rather than SMR itself.     

Gill Morphometry in Growth Hormone Transgenic Pacific Coho Salmon,Onchorhynchus kisutch,Differs Markedly from that in GH Transgenic Atlantic Salmon

In a previous study we showed that many of the morphological features of the respiratory system of GH (growth hormone) transgenic Atlantic salmon are greater than similarly sized control salmon. Here we show that the manifestation of GH transgene is similar in two different lines of GH transgenic Pacific coho salmon, but that it is very different from that in the GH transgenic Atlantic salmon. The GH transgenic Pacific coho salmon do not have a larger gill surface area than similarly sized control fish.     

Disease resistance, stress response and effects of triploidy in growth hormone transgenic coho salmon

Diploid and triploid coho salmon Oncorhynchus kisutch transgenic for growth hormone (GH) and control coho salmon were compared for differences in disease resistance and stress response. Resistance to the bacterial pathogen Vibrio anguillarum was not affected in transgenic fish relative to their non‐transgenic counterparts when they were infected at the fry stage, but was lower in transgenic fish when infected near smolting. Vaccination against vibriosis provided equal protection to both transgenic and non‐transgenic fish. Triploid fish showed a lower resistance to vibriosis than their diploid counterparts. Diploid transgenic fish and non‐transgenic fish appeared to show similar physiological and cellular stress responses to a heat shock. These studies provide information useful for both performance and ecological risk assessments of growth‐accelerated coho salmon.     

Inside the heads of David and Goliath: environmental effects on brain morphology among wild and growth-enhanced coho salmon Oncorhynchus kisutch

Transgenic and wild-type individual coho salmon Oncorhynchus kisutch were reared in hatchery and near-natural stream conditions and their brain and structure sizes were determined. Animals reared in the hatchery grew larger and developed larger brains, both absolutely and when controlling for body size. In both environments, transgenics developed relatively smaller brains than wild types. Further, the volume of the optic tectum of both genotypes was larger in the hatchery animals and the cerebellum of transgenics was smaller when reared in near-natural streams. Finally, wild types developed a markedly smaller telencephalon under hatchery conditions. It is concluded that, apart from the environment, genetic factors that modulate somatic growth rate also have a strong influence on brain size and structure.     

Gut size in GH‐transgenic coho salmon is enhanced by both the GHtransgene and increased food intake

Growth hormone transgenic coho salmon Oncorhynchus kisutch fed at the same ration level as non‐transgenic controls (Tc) had the same growth rate as non‐transgenic controls (Nt). In contrast, growth hormone transgenic coho salmon (Tf) fed ad libitum ate about twice as much and had much higher growth rates than the other two groups. The most obvious result was the significantly larger caeca in the Tf group relative to both Nt or pair‐fed Tc. The Tf fish had more caeca that were longer. The results suggested that the effect was indirect and the enlarged caeca required both the GHtransgene and hyperphagia to cause enlarged caecal capacity. A small part of the results, however, also suggested that there was a direct effect of the GHtransgene on some gut tissues, particularly the intestine.     

Early Life-History Consequences of Growth-Hormone Transgenesis in Rainbow Trout Reared in Stream Ecosystem Mesocosms

There is persistent commercial interest in the use of growth modified fishes for shortening production cycles and increasing overall food production, but there is concern over the potential impact that transgenic fishes might have if ever released into nature. To explore the ecological consequences of transgenic fish, we performed two experiments in which the early growth and survival of growth-hormone transgenic rainbow trout (Oncorhynchus mykiss) were assessed in naturalized stream mesocosms that either contained predators or were predator-free. We paid special attention to the survival bottleneck that occurs during the early life-history of salmonids, and conducted experiments at two age classes (first-feeding fry and 60 days post-first-feeding) that lie on either side of the bottleneck. In the late summer, the first-feeding transgenic trout could not match the growth potential of their wild-type siblings when reared in a hydrodynamically complex and oligotrophic environment, irrespective of predation pressure. Furthermore, overall survival of transgenic fry was lower than in wild-type (transgenic = 30% without predators, 8% with predators; wild-type = 81% without predators, 31% with predators). In the experiment with 60-day old fry, we explored the effects of the transgene in different genetic backgrounds (wild versus domesticated). We found no difference in overwinter survival but significantly higher growth by transgenic trout, irrespective of genetic background. We conclude that the high mortality of GH-transgenic trout during first-feeding reflects an inability to sustain the basic metabolic requirements necessary for life in complex, stream environments. However, when older, GH-transgenic fish display a competitive advantage over wild-type fry, and show greater growth and equal survival as wild-type. These results demonstrate how developmental age and time of year can influence the response of genotypes to environmental conditions. We therefore urge caution when extrapolating the results of GH-transgenesis risk assessment studies across multiple life-history or developmental stages.     

Adaptive trade-offs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams

1. Adaptive trade-offs are fundamental to the evolution of diversity and the coexistence of similar taxa and occur when complimentary combinations of traits maximize efficiency of resource exploitation or survival at different points on environmental gradients. 2. Standard metabolic rate (SMR) is a key physiological trait that reflects adaptations to baseline metabolic performance, whereas active metabolism reflects adaptations to variable metabolic output associated with performance related to foraging, predator avoidance, aggressive interactions or migratory movements. Benefits of high SMR and active metabolism may change along a resource (productivity) gradient, indicating that a trade-off exists among active metabolism, resting metabolism and energy intake. 3. We measured and compared SMR, maximal metabolic rate (MMR), aerobic scope (AS), swim performance (UCrit) and growth of juvenile hatchery and wild steelhead and coho salmon held on high- and low-food rations in order to better understand the potential significance of variation in SMR to growth, differentiation between species, and patterns of habitat use along a productivity gradient. 4. We found that differences in SMR, MMR, AS, swim performance and growth rate between steelhead trout and coho salmon were reduced in hatchery-reared fish compared with wild fish. Wild steelhead had a higher MMR, AS, swim performance and growth rate than wild coho, but adaptations between species do not appear to involve differences in SMR or to trade-off increased growth rate against lower swim performance, as commonly observed for high-growth strains. Instead, we hypothesize that wild steelhead may be trading off higher growth rate for lower food consumption efficiency, similar to strategies adopted by anadromous vs. resident brook trout and Atlantic salmon vs. brook trout. This highlights potential differences in food consumption and digestion strategies as cryptic adaptations ecologically differentiating salmonid species. 5. We hypothesize that divergent digestive strategies, which are common and well documented among terrestrial vertebrates, may be an important but overlooked aspect of adaptive strategies of juvenile salmonids, and fish in general.