Maladaptation and phenotypic mismatch in cultured Atlantic salmon used for stocking

Compared to wild populations, cultured Atlantic salmon often sustain higher mortality rates and lower adult return rates when stocked as juveniles into natural streams. The ultimate causes for such differences in fitness, however, are not clear. Here we tested if relaxed levels of natural selection and improved survival in the hatchery environment could account for the observed degree of maladaptation among stocked fish. To do this, we assessed the degree of phenotypic mismatch between wild and cultured fish in three populations over five consecutive years. Significant differences were found in several phenotypic traits that are likely to have fitness implications. Thus, if the objective is to mimic wild individuals for restoration purposes, current hatchery practices aimed at maximising juvenile survival and enhancing growth may need to be revised.     

Rainbow trout in seasonal environments: phenotypic trade‐offs across a gradient in winter duration

Survival through periods of resource scarcity depends on the balance between metabolic demands and energy storage. The opposing effects of predation and starvation mortality are predicted to result in trade‐offs between traits that optimize fitness during periods of resource plenty (e.g., during the growing season) and those that optimize fitness during periods of resource scarcity (e.g., during the winter). We conducted a common environment experiment with two genetically distinct strains of rainbow trout to investigate trade‐offs due to (1) the balance of growth and predation risk related to foraging rate during the growing season and (2) the allocation of energy to body size prior to the winter. Fry (age 0) from both strains were stocked into replicate natural lakes at low and high elevation that differed in winter duration (i.e., ice cover) by 59 days. Overwinter survival was lowest in the high‐elevation lakes for both strains. Activity rate and growth rate were highest at high elevation, but growing season survival did not differ between strains or between environments. Hence, we did not observe a trade‐off between growth and predation risk related to foraging rate. Growth rate also differed significantly between the strains across both environments, which suggests that growth rate is involved in local adaptation. There was not, however, a difference between strains or between environments in energy storage. Hence, we did not observe a trade‐off between growth and storage. Our findings suggest that intrinsic metabolic rate, which affects a trade‐off between growth rate and overwinter survival, may influence local adaptation in organisms that experience particularly harsh winter conditions (e.g., extended periods trapped beneath the ice in high‐elevation lakes) in some parts of their range.     

Influences of life history and environment on lake trout (Salvelinus namaycush) growth and longevity in the Husky Lakes of the Western Canadian Arctic

The interaction between an organism and its environment is a major determinant of an individual’s growth rate, longevity, and fitness. Such interactions and resultant variation in growth is particularly prevalent in salmonids where a diversity of life history types and morphotypes can be observed within a single ecosystem. Lake trout, Salvelinus namaycush, are typically considered freshwater residents. However, three life history types within the Husky Lakes estuary and connected lakes, NWT were recently documented, including semi-anadromous, brackish-water resident, and freshwater resident. To understand how use of brackish-water environments influences growth and longevity in lake trout, we assessed otolith increment widths, as a proxy for annual fish growth, and age-at- capture among life history types. Assessment of increments indicated that growth increased in brackish water for semi-anadromous lake trout, and that growth was faster for semi-anadromous and brackish-water residents than for freshwater residents (70 mm larger on average at age 15). In addition, age at capture was significantly older in brackish-water residents (3.8 years older) when compared to the other life histories. Together these results indicate that life in brackish water can have positive effects on growth and longevity for lake trout.

     

Within-population heterogeneity of habitat use by lake trout Salvelinus namaycush

To learn more about the degree of individual variation in resource use by lake trout Salvelinus namaycush , ultrasonic telemetry was used to study their habitat use in a lake without pelagic schooling fish prey. Individuals spent most of their time within the metalimnion in favourable water temperatures. They also made frequent excursions, however, into lake temperatures exceeding their optimum for physiological performance at all temporal scales considered. Their frequent use of nearshore habitats suggested that feeding in littoral areas may be common. Habitat use was highly variable among individuals, but spatial habitat use by individuals showed remarkable consistency between years. In particular, some lake trout exhibited high site fidelity to shallow, nearshore areas, whereas others used deep areas extensively. This level of between-individual variation indicated niche partitioning by depth and the possibility of alternative foraging strategies.     

The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta)

This study addressed two hypotheses: (1) that individual recognitionis used to reduce the cost of contesting resources in sea troutand (2) that the hatchery environment selects against individualrecognition. Predictions from these hypotheses were tested inlaboratory experiments where behavior and growth were studiedin juvenile sea trout. In tact groups of familiar fish werecompared with groups that contained both familiar and unfamiliarindividuals. In general, the results were in agreement withthe first hypothesis. Familiar fish in intact groups had morestable dominance ranks, higher food intake, and better utilizationof food. Familiarity also reduced the distance to the nearestneighbor. Furthermore, initiators of conflicts were more likelyto win against familiar fish than against strangers. These resultssupport game-theory-based hypotheses explaining the dear-enemyphenomenon as an effect of familiarity A picture emerges inwhich familiarity stabilizes the hierarchical structure of agroup and governs behavioral modifications that will promotefeeding and growth, in turn leading to higher fitness. The secondhypothesis, which predicted a reduced effect of individual recognitionin sea-ranched trout, was not strongly supported because familiarityaffected sea-ranched and wild trout similarly in most respects.However, familiarity was not beneficial for growth in sea-ranchedtrout, whereas it increased growth rate in wild fish. In addition,sea-ranched trout tended to maintain larger distances to theirnearest neighbors than did wild trout.     

Inbreeding, outbreeding and environmental effects on genetic diversity in 46 walleye (Sander vitreus) populations

Genetic diversity is recognized as an important population attribute for both conservation and evolutionary purposes; however, the functional relationships between the environment, genetic diversity, and fitness-related traits are poorly understood. We examined relationships between selected lake parameters and population genetic diversity measures in 46 walleye (Sander vitreus) populations across the province of Ontario, Canada, and then tested for relationships between six life history traits (in three categories: growth, reproductive investment, and mortality) that are closely related to fitness, and genetic diversity measures (heterozygosity, d2, and Wright's inbreeding coefficient). Positive relationships were observed between lake surface area, growing degree days, number of species, and hatchery supplementation versus genetic diversity. Walleye early growth rate was the only life history trait significantly correlated with population heterozygosity in both males and females. The relationship between FIS and male early growth rate was negative and significant (P < 0.01) and marginally nonsignificant for females (P = 0.06), consistent with inbreeding depression effects. Only one significant relationship was observed for d2: female early growth rate (P < 0.05). Stepwise regression models showed that surface area and heterozygosity had a significant effect on female early growth rate, while hatchery supplementation, surface area and heterozygosity had a significant effect on male early growth rate. The strong relationship between lake parameters, such as surface area, and hatchery supplementation, versus genetic diversity suggests inbreeding and outbreeding in some of the populations; however, the weak relationships between genetic diversity and life history traits indicate that inbreeding and outbreeding depression are not yet seriously impacting Ontario walleye populations.     

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.     

Heart rate responses to predation risk in Salmo trutta are affected by the rearing environment

Both wild‐ and hatchery‐reared brown trout Salmo trutta , 18 months of age and of the same genetic origin, responded with increased heart rates (tachycardia) to a simulated predator attack on 2 consecutive days. Brown trout reared in the hatchery showed a more rapidly induced tachycardia compared with wild‐reared fish at day 1, but not day 2. During an undisturbed period several hours after attacks, hatchery‐reared brown trout maintained higher heart rates compared to wild‐reared fish on both days. Behavioural responses to the attack were very low for all fish, although hatchery‐reared fish tended to be more active than wild fish after the attack day 2. The observed differences may have had a genetic background caused by different selection regimes in the hatchery‐ and wild‐rearing environments, or could have been due to different phenotypic responses in the two environments.     

Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality

The magnitude of fitness variation caused by maternal effects and, thus, the adaptive significance of maternal traits may depend on environmental quality, generating crossing reaction norms among offspring phenotypes that shape life-history evolution. By manipulating intraclutch variation in egg size and comparing siblings we examined the maternal effects of egg size on offspring performance and tested for the existence of reaction norms to environmental quality using the brown trout Salmo trutta. When sibling groups of small and large eggs were reared separately in a hatchery environment initial size differences disappeared rapidly. However, in semi-natural environments and under direct competition, juveniles from large eggs experienced growth and survival advantages over siblings from small eggs. Moreover, distinct reaction norms existed, with the differences in performance of juveniles from small and large eggs being most pronounced in the poorer growth environments. Our results provide the first direct evidence, to our knowledge, for a causal relationship between egg size and fitness-related traits in fishes, independent of potentially confounding genetic effects. Moreover, they indicate that previous studies have been biased by experimental conditions that excluded competitive asymmetries and environmental variability. The existence of reaction norms indicates a shift in optimal egg size across gradients of environmental quality that probably shapes the evolution of this trait.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Environment-phenotype interactions: Influences of brackish-water rearing on lake trout (<Emphasis Type="Italic">Salvelinus namaycush</Emphasis>) physiology

Fertilization and development in salmonids occurs almost exclusively within freshwater environments (< 1 ppt). A less common life history strategy in this group of fishes is the brackish-water resident life history, where entire life cycles occur in brackish water (> 1 ppt). In the present study, we tested the hypothesis that differences in rearing environment (fresh or brackish water) results in significant differences in the ability of lake trout to ionoregulate when faced with a salinity challenge later in life. To test this, genetically similar lake trout were fertilized and raised at either 0 or 5 ppt saltwater. At approximately 240 days post hatch, lake trout from both rearing environments were acutely transferred to 20 ppt salt water or their respective rearing environments as a control. Individuals were sampled at time 0, 1, 7, and 14 days post transfer. Fish raised in 5 ppt transferred to 20 ppt saltwater had significantly higher gill Na⁺ K⁺-ATPase activity, gill Na⁺ K⁺-ATPase α1b expression, and lower plasma osmolality when compared to freshwater reared lake trout transferred to 20 ppt across various time points. Additionally, the 5 ppt control treatment had greater overall aerobic scope than 0 ppt control fish and those transferred from 0 ppt to 20 ppt. These data imply that populations exhibiting a brackish-water resident life history, as has been observed in Arctic Canada, may have an advantage over freshwater reared conspecifics when foraging in marine influenced environments and colonizing new locations in coastal regions.     

Growth and social interactions of wild and sea-ranched brown trout and their hybrids

A laboratory study of the social behaviour and growth performance of juvenile brown trout Salmo trutta of wild and sea-ranched origin and their crosses, indicated that the social behaviour of wild and sea-ranched fish differed. Male and female parents seemed to have a different impact on the juveniles. The category having wild mother and sea-ranched father were less aggressive, less active in general, but active in feeding, and therefore had higher growth rates. This pattern arose despite that the feeding rate and the motivation to first get a food item when food was provided did not differ between the groups of fish. Wild fish tended to be most aggressive. If sea-ranched and wild fish have different intrinsic (genetically based) 'life styles', the crosses between wild and sea-ranched fish indicate that there is likelihood for an introgression of genes adapted to hatchery environment into the genetics of wild conspecifics. This is particularly serious when hatchery-reared fish invades wild populations over many years.     

Phenotypic convergence of artificially reared and wild trout is mediated by shape plasticity

Phenotypic plasticity can be viewed as the first level of defense of organism homeostasis against environmental stress and therefore represents the potential to deal with rapid environmental changes. Transitions between low complexity, artificial environments and complex, natural habitats can promote phenotypic plasticity. Here, we conducted an experimental introduction with juvenile brown trout to evaluate the plasticity of shape in response to a transition between contrasting environments. We released 202 juvenile trout reared under hatchery conditions in a natural stream and analyzed changes in shape and morphological variability after 5 months. A geometric morphometrics approach based on 14 landmarks was used to compare changes in body shape for 37 fish recaptured at the end of the experiment. A similar number of hatchery and wild fish caught at the receptor stream were used as controls for shape in the two environments. After 5‐months, fish showed significant change in shape, shifting from elongated to robust shapes, and affecting to the relative position of the caudal peduncle. These new shapes were closer to wild than to the hatchery shapes, suggesting a process of rapid phenotype change. Moreover, these changes were concomitant with a marked increase in morphological variability. Our results support the hypothesis that phenotypic plasticity is a major potential for adjustment to environmental change but not the idea that shape can be constrained by initial shapes. We confirmed the “increased” variance hypothesis and phenotype convergence with wild morphs. This has important implications because stresses the role of phenotypic plasticity as a buffer that allows organisms to cope with important environmental discontinuities at time scales that preclude the onset of adaptive adjustments. We suggest that environmental conditioning and shape plasticity can overcome both reduced morphological diversity and phenotype uncoupling with habitat characteristics resulting from initial rearing in low complexity artificial environments.     

Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations

Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.     

Impact of live food on survival and growth of hatchery‐reared sea trout (Salmo trutta trutta L.) parr in the wild

Survival rates and growth parameters of hatchery‐reared sea trout (Salmo trutta trutta L.) fry were determined after stocking in the wild. The larvae were hatchery‐reared for 12 weeks in two groups: fry were fed either on live zooplankton and live chironomidae larvae (LFG), or fed a pellet diet (PFG). The survival rate and specific growth rates were higher in the LFG than in the PFG group. Most effective for hatchery‐reared fish intended for stocking was the natural, live feed. The mean number of chironomid larvae found in the stomachs of fish that were initially captured in the wild was significantly higher in the LFG than in the PFG group. The live diet supplied in the rearing period had a positive impact on the foraging skills of the sea trout fry and their survival in the wild after their release on 24 April 2010.     

Who are the missing parents? Grandparentage analysis identifies multiple sources of gene flow into a wild population

In order to increase the size of declining salmonid populations, supplementation programmes intentionally release fish raised in hatcheries into the wild. Because hatchery-born fish often have lower fitness than wild-born fish, estimating rates of gene flow from hatcheries into wild populations is essential for predicting the fitness cost to wild populations. Steelhead trout (Oncorhynchus mykiss) have both freshwater resident and anadromous (ocean-going) life history forms, known as rainbow trout and steelhead, respectively. Juvenile hatchery steelhead that 'residualize' (become residents rather than go to sea as intended) provide a previously unmeasured route for gene flow from hatchery into wild populations. We apply a combination of parentage and grandparentage methods to a three-generation pedigree of steelhead from the Hood River, Oregon, to identify the missing parents of anadromous fish. For fish with only one anadromous parent, 83% were identified as having a resident father while 17% were identified as having a resident mother. Additionally, we documented that resident hatchery males produced more offspring with wild anadromous females than with hatchery anadromous females. One explanation is the high fitness cost associated with matings between two hatchery fish. After accounting for all of the possible matings involving steelhead, we find that only 1% of steelhead genes come from residualized hatchery fish, while 20% of steelhead genes come from wild residents. A further 23% of anadromous steelhead genes come from matings between two resident parents. If these matings mirror the proportion of matings between residualized hatchery fish and anadromous partners, then closer to 40% of all steelhead genes come from wild trout each generation. These results suggest that wild resident fish contribute substantially to endangered steelhead 'populations' and highlight the need for conservation and management efforts to fully account for interconnected Oncorhynchus mykiss life histories.     

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.     

Parallel and non‐parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus)

Parallel phenotypic evolution occurs when independent populations evolve similar traits in response to similar selective regimes. However, populations inhabiting similar environments also frequently show some phenotypic differences that result from non‐parallel evolution. In this study, we quantified the relative importance of parallel evolution to similar foraging regimes and non‐parallel lake‐specific effects on morphological variation in European whitefish (Coregonus lavaretus). We found evidence for both lake‐specific morphological characteristics and parallel morphological divergence between whitefish specializing in feeding on profundal and littoral resources in three separate lakes. Foraging specialists expressed similar phenotypes in different lakes in both overall body shape and selected measured morphological traits. The morphology of the two whitefish specialists resembled that predicted from other fish species, supporting the conclusion of an adaptive significance of the observed morphological characteristics. Our results indicate that divergent natural selection resulting from foraging specialization is driving and/or maintaining the observed parallel morphological divergence. Whitefish in this study may represent an early stage of divergence towards the evolution of specialized morphs.     

Costs of inducible defence along a resource gradient

In addition to having constitutive defence traits, many organisms also respond to predation by phenotypic plasticity. In order for plasticity to be adaptive, induced defences should incur a benefit to the organism in, for example, decreased risk of predation. However, the production of defence traits may include costs in fitness components such as growth, time to reproduction, or fecundity. To test the hypothesis that the expression of phenotypic plasticity incurs costs, we performed a common garden experiment with a freshwater snail, Radix balthica, a species known to change morphology in the presence of molluscivorous fish. We measured a number of predator-induced morphological and behavioural defence traits in snails that we reared in the presence or absence of chemical cues from fish. Further, we quantified the costs of plasticity in fitness characters related to fecundity and growth. Since plastic responses may be inhibited under limited resource conditions, we reared snails in different densities and thereby levels of competition. Snails exposed to predator cues grew rounder and thicker shells, traits confirmed to be adaptive in environments with fish. Defence traits were consistently expressed independent of density, suggesting strong selection from predatory molluscivorous fish. However, the expression of defence traits resulted in reduced growth rate and fecundity, particularly with limited resources. Our results suggest full defence in predator related traits regardless of resource availability, and costs of defence consequently paid in traits related to fitness.