Egg size and emergence timing affect morphology and behavior in juvenile Chinook Salmon,Oncorhynchus tshawytscha

Variation in early life history traits often leads to differentially expressed morphological and behavioral phenotypes. We investigated whether variation in egg size and emergence timing influence subsequent morphology associated with migration timing in juvenile spring Chinook Salmon, Oncorhynchus tshawytscha. Based on evidence for a positive relationship between growth rate and migration timing, we predicted that fish from small eggs and fish that emerged earlier would have similar morphology to fall migrants, while fish from large eggs and individuals that emerged later would be more similar to older spring yearling migrants. We sorted eyed embryos within females into two size categories: small and large. We collected early and late‐emerging juveniles from each egg size category. We used landmark‐based geometric morphometrics and found that egg size appears to drive morphological differences. Egg size shows evidence for an absolute rather than relative effect on body morphology. Fish from small eggs were morphologically more similar to fall migrants, while fish from large eggs were morphologically more similar to older spring yearling migrants. Previous research has shown that the body morphology of fish that prefer the surface or bottom location in a tank soon after emergence also correlates with the morphological variations between wild fall and spring migrants, respectively. We found that late‐emerging fish spent more time near the surface. Our study shows that subtle differences in early life history characteristics may correlate with a diversity of future phenotypes.     

State-dependent shifts between nocturnal and diurnal activity in salmon

Animal species have usually evolved to be active at a specific time of the daily cycle, and so are either diurnal, nocturnal or crepuscular. However, we show here that the daily timing of activity in juvenile Atlantic salmon is related to the life-history strategy that they have adopted (i.e. the age at which they will migrate to the sea) and their current state (body size/relative nutritional state). Salmon can detect food more easily by day than by night, but the risk of predation is greater. Nocturnal foraging should generally be preferred, but the greater the need for growth, the greater should be the shift towards diurnal activity. In line with this prediction, all fish were predominantly nocturnal, but salmon preparing to migrate to the sea, which would experience size-dependent mortality during the forthcoming migration, were more diurnal than fish of the same age and size that were delaying migration for a further year. Moreover, the proportion of activity by day was negatively correlated with body size within the intending migrants. It has previously been shown that overwinter survival in fish delaying migration is maximized not by growth but by minimizing exposure to predators. As predicted, daytime activity in these fish was correlated with the prior rate of weight loss, fish being more diurnal when their risk of starvation was greater. To our knowledge, these are the first quantitative demonstrations of state-dependent variation in the timing of daily activity.     

Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

Accumulating evidence suggests that within‐individual plasticity of behavioural and physiological traits is limited, resulting in stable among‐individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross‐generational effects. Patterns of trait covariation, among‐individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among‐individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour–physiology interactions.     

The relationships between specific dynamic action,nutrient retention and feed conversion ratio in farmed freshwater Chinook salmon (Oncorhynchus tshawytscha)

Improving the feed conversion ratio (FCR; the amount of feed consumed relative to the amount of weight gain) can reduce both production costs and environmental impacts of farmed fish. The aim of this study was to investigate what drives FCR to understand how nutrients are retained, as well as the amount of oxygen consumed for digestion, absorption and assimilation (a metabolic process known as specific dynamic action, SDA). Feed-efficient and inefficient Chinook salmon (Oncorhynchus tshawytscha) in fresh water were identified using ballotini beads and X-radiography that tracked individual feed intake across three assessment periods under satiated feeding. This allowed a comparison of physiological traits and body composition between the two FCR phenotypes over two time points as Chinook salmon grew from 305 to 620 g. Fish with higher daily feed intake (DFI) had higher daily weight gain (DWG) as expected. Nonetheless, the relationship between FCR and DFI as well as FCR and DWG was variable between time points. FCR and DWG were not correlated at the first time point and were negatively correlated at the second time point. In contrast, FCR and DFI were positively correlated at the first time point but not the second. Despite this, efficient fish ate smaller meals and retained more protein, lipid and energy in their body tissues. There was no detectable difference in metabolism between the two FCR phenotypes with respect to minimal resting metabolic rate, maximum metabolic rate, aerobic scope, or SDA parameters. In conclusion, FCR is not consistently associated with growth and metabolic differences in freshwater Chinook salmon, but FCR-efficient fish retain more nutrients and consume smaller meals.     

Swimming performance and morphology of juvenile sockeye salmon, <Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>: comparison of inlet and outlet fry populations

We raised two populations of sockeye salmon fry from fertilized eggs in the laboratory and tested the hypothesis that outlet fry populations, fish which must migrate upstream to reach rearing lakes after yolk-sac absorption, have better swimming ability and morphological characteristics conducive to enhanced swimming performance than inlet fry populations, fish which migrate downstream to rearing lakes. Despite being of identical age, fry from the outlet population were larger (approx. 6.7% longer, ~5 mm on average) and more laterally compressed than inlet fry at the time of our initial experiments. Using an open-top box flume, we found that the burst-swimming performance (in cm s⁻¹) of the outlet population was 31% better. We found no differences between populations in prolonged-swimming performance. We were unable to find any direct relationships between measures of swimming performance and size or shape variables, suggesting that the larger, more robust morphology of outlet fry was not responsible for the superior burst ability. Recent biochemical studies indicate outlet fry may be metabolically better provisioned for burst swimming than inlet fry. It is possible that the morphological differences between the populations of fry reflect adaptations needed by adults during their migration and spawning.     

Microsatellite variation reveals weak genetic structure and retention of genetic variability in threatened Chinook salmon (<Emphasis Type="Italic">Oncorhynchus tshawytscha</Emphasis>) within a Snake River watershed

Pacific salmon (Oncorhynchus spp.) have been central to the development of management concepts associated with evolutionarily significant units (ESUs), yet there are still relatively few studies of genetic diversity within threatened and endangered ESUs for salmon or other species. We analyzed genetic variation at 10 microsatellite loci to evaluate spatial population structure and genetic variability in indigenous Chinook salmon (Oncorhynchus tshawytscha) across a large wilderness basin within a Snake River ESU. Despite dramatic 20th century declines in abundance, these populations retained robust levels of genetic variability. No significant genetic bottlenecks were found, although the bottleneck metric (M ratio) was significantly correlated with average population size and variability. Weak but significant genetic structure existed among tributaries despite evidence of high levels of gene flow, with the strongest genetic differentiation mirroring the physical segregation of fish from two sub-basins. Despite the more recent colonization of one sub-basin and differences between sub-basins in the natural level of fragmentation, gene diversity and genetic differentiation were similar between sub-basins. Various factors, such as the (unknown) genetic contribution of precocial males, genetic compensation, lack of hatchery influence, and high levels of current gene flow may have contributed to the persistence of genetic variability in this system in spite of historical declines. This unique study of indigenous Chinook salmon underscores the importance of maintaining natural populations in interconnected and complex habitats to minimize losses of genetic diversity within ESUs.     

Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha

Recent studies suggest that hatchery-reared fish can have smaller brain-to-body size ratios than wild fish. It is unclear, however, whether these differences are due to artificial selection or instead reflect differences in rearing environment during development. Here we explore how rearing conditions influence the development of two forebrain structures, the olfactory bulb and the telencephalon, in juvenile Chinook salmon (Oncorhynchus tshawytscha) spawned from wild-caught adults. First, we compared the sizes of the olfactory bulb and telencephalon between salmon reared in a wild stream vs. a conventional hatchery. We next compared the sizes of forebrain structures between fish reared in an enriched NATURES hatchery and fish reared in a conventional hatchery. All fish were size-matched and from the same genetic cohort. We found that olfactory bulb and telencephalon volumes relative to body size were significantly larger in wild fish compared to hatchery-reared fish. However, we found no differences between fish reared in enriched and conventional hatchery treatments. Our results suggest that significant differences in the volume of the olfactory bulb and telencephalon between hatchery and wild-reared fish can occur within a single generation.     

Allometric relationships in morphological traits associated with foraging,swimming ability,and predator defense reveal adaptations toward brackish and freshwater environments in the threespine stickleback

Freshwater colonization by threespine stickleback has led to divergence in morphology between ancestral marine and derived freshwater populations, making them ideal for studying natural selection on phenotypes. In an open brackish–freshwater system, we previously discovered two genetically distinct stickleback populations that also differ in geometric shape: one mainly found in the brackish water lagoon and one throughout the freshwater system. As shape and size are not perfectly correlated, the aim of this study was to identify the morphological trait(s) that separated the populations in geometric shape. We measured 23 phenotypes likely to be important for foraging, swimming capacity, and defense against predation. The lateral plate morphs in freshwater displayed few significant changes in trait sizes, but the low plated expressed feeding traits more associated with benthic habitats. When comparing the completely plated genetically assigned populations, the freshwater, the hybrids, the migrants and the lagoon fish, many of the linear traits had different slopes and intercepts in trait‐size regressions, precluding our ability to directly compare all traits simultaneously, which most likely results from low variation in body length for the lagoon and migrant population. We found the lagoon stickleback population to be more specialized toward the littoral zone, displaying benthic traits such as large, deep bodies with smaller eyes compared to the freshwater completely plated morph. Further, the lagoon and migrant fish had an overall higher body coverage of lateral plates compared to freshwater fish, and the dorsal and pelvic spines were longer. Evolutionary constraints due to allometric scaling relationships could explain the observed, overall restricted, differences in morphology between the sticklebacks in this study, as most traits have diversified in common allometric trajectories. The observed differences in foraging and antipredation traits between the fish with a lagoon and freshwater genetic signature are likely a result of genetic or plastic adaptations toward brackish and freshwater environments.     

The effects of paternal reproductive tactic and rearing environment on juvenile variation in growth as mediated through aggression and foraging behaviours of Chinook salmon (Oncorhynchus tshawytscha)

In species with indeterminate growth, differential growth rates can lead to animals adopting alternative reproductive tactics such as sneak–guard phenotypes, which is partially predicted by variation in growth during the juvenile life‐history stage. To investigate sources of growth variation, we examined the independent and joint effects of paternal reproductive tactic (G) and rearing environment (E) on juvenile growth in Chinook salmon (Oncorhynchus tshawytscha), hypothesizing G and E effects are partially mediated through differences in behaviour such as aggressive interactions and resulting foraging behaviours. We created maternal half‐sibling families with one‐half of the female's eggs fertilized by the milt of a sneaker “jack” and the other half by a guarder “hooknose”. At the exogenous feeding stage, each split‐clutch family was then divided again and reared in a rationed diet or growth‐promotion diet environment for approximately 6 months, during which growth parameters were measured. Before saltwater transfer at 9 months of age, social interactions were observed in groups of six fish of various competitor origins. We found ration restricts growth rate and juvenile mass, and evidence of genetic effects on growth depensation, where jack‐sired individuals grew less uniformly over time. These growth‐related differences influenced an individual's level of aggression, with individuals raised on a restricted diet and those whose families experienced greatest growth being most aggressive. These individuals were more likely to feed than not and feed most often. Jack‐sired individuals were additionally aggressive in the absence of food, and when raised on a rationed diet outcompeted others to feed most. These results show how individuals may achieve higher growth rates via intrinsic (G) or induced (E) aggressive behavioural phenotypes, and eventually attain the threshold body size necessary during the saltwater phase to precociously sexually mature and adopt alternative reproductive phenotypes.     

Trade-off between growth rate and aggression in juvenile coho salmon, Oncorhynchus kisutch

In juvenile salmon and trout, there seems to be a positive phenotypic correlation between individual aggression level and growth rate. Aggressive fish are dominant, and they obtain and defend territories, giving them access to good feeding sites. Being aggressive may increase predation risk, and may also carry costs such as increased metabolic demand, with effects on growth. To test the hypothesis that there is a trade-off between individual growth rate and aggression, we mated 12 female coho salmon with two unique males each, creating 24 full-sibling families. Growth of individually marked fish from each family was estimated in a situation where food could not be monopolized. Thereafter, individual fish were tested for mirror-elicited agonistic behaviour. We found significant variation between families in early growth rate, with a high heritability (1.04). There was also significant between-family variation in agonistic behaviour, but activity was generally low and heritability was low (0.25) and not significant. Growth rate and agonistic behaviour were negatively correlated. These results imply that aggressive behaviour has an energetic cost. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (<Emphasis Type="Italic">Podarcis melisellensis</Emphasis>)

If alternative phenotypes in polymorphic populations do not mate randomly, they can be used as model systems to study adaptive diversification and possibly the early stages of sympatric speciation. In this case, non random mating is expected to support genetic divergence among the different phenotypes. In the present study, we use population genetic analyses to test putatively neutral genetic divergence (of microsatellite loci) among three colour morphs of the lizard Podarcis melisellensis, which is associated with differences in male morphology, performance and behaviour. We found weak evidence of genetic divergence, indicating that gene flow is somewhat restricted among morphs and suggesting possible adaptive diversification.     

Spatio-temporal dynamics of alternative male phenotypes in coho salmon populations in response to ocean environment

1. The coexistence of alternative reproductive phenotypes will probably be shaped by spatial and temporal variability in the environment. However, the effects of such variability on coexistence and the scale at which it operates are seldom understood. 2. To quantify such effects, we examined spatial and temporal dynamics in the abundance and frequency of alternative phenotypes of male coho salmon, Oncorhynchus kisutch Walbaum, which mature as either large fighters (age-3 'hooknoses') or small sneakers (age-2 'jacks'). Using over 20 years of data on coded-wire tagged fish released from nine Oregon hatcheries, we tested for the effects of ocean environment independent of those due to freshwater rearing. 3. Annual fluctuations of the abundance of jack and hooknose males within populations were correlated strongly by brood year (cohort) but not by return year (breeding group). This occurred independently of significant effects of release practice (i.e. the number of fish released, body size at release and date of release), indicating that a synchronized fluctuation in mortality during the first year at sea was the predominant cause. As a result, the annual frequency of the alternative phenotypes at breeding varied considerably within populations. 4. Spatial patterns in the annual fluctuations of the two phenotypes were similar (i.e. synchronous among populations), except that jacks showed local spatial structure (decreased synchrony with distance) not evident among hooknoses. This suggests that oceanic processes affecting the two phenotypes operate at different spatial scales. Despite effects on salmon abundance, the ocean environment had little influence through its effects on salmon growth on the relative frequencies of the alternative phenotypes within and among populations. 5. The results provide insight into the evolutionary dynamics of alternative phenotypes, including an intragenerational time lag that increases annual variability in phenotype frequencies at breeding (return years) and the significance of local freshwater processes, rather than oceanic processes, on phenotype expression. Freshwater processes, such as juvenile growth, timing of migration and breeding competition, operating at evolutionary and intragenerational time-scales, are probably the predominant forces affecting phenotype frequency.     

Maladaptation and phenotypic mismatch in hatchery‐reared Atlantic salmon Salmo salar released in the wild

Changes in body shape, fluctuating asymmetry (FA) and crypsis were compared among Atlantic salmon Salmo salar fry kept as controls in captivity and those released and subsequently recaptured in the wild according to a before‐after‐control‐impact (BACI) design. Hatchery fish that survived in the wild became more cryptic and displayed a much lower incidence of fin erosion and of asymmetric individuals than control fish kept in captivity. Significant differences in body shape were also apparent, and survivors had longer heads, thicker caudal peduncles and a more streamlined body shape than hatchery controls as early as 20 days following stocking, most likely as a result of phenotypic plasticity and non‐random, selective mortality of maladapted phenotypes. Hatchery‐reared fish typically perform poorly in the wild and the results of this study indicate that this may be due to phenotypic mismatch, i.e. because hatcheries generate fish that are phenotypically mismatched to the natural environment.     

Size‐dependent thermal preferences in a pelagic fish

Large fish often inhabit colder waters than small fish. Using a simple bioenergetic model, we found that the optimal temperature for growth should decrease with increasing body size. We predicted that this mechanism would produce an ontogenetic change in thermal preference and then tested our predictions with Pacific salmon, Oncorhynchus spp. In a laboratory experiment, the slope of a regression of growth increment on initial size became steeper with increasing temperature, so that the optimal temperature for growth decreased with increasing body size. In field observations, larger and older salmon inhabited cooler areas, whereas smaller and younger salmon inhabited warmer areas. These patterns were consistent with a size‐dependent effect of temperature on condition factor, a parameter shown experimentally to be a measure of the most recent growth performance. Temperatures for maximising condition factor were lower for larger fish. Thus, an ontogenetic change in individual thermal preference toward cooler areas maximises the growth performance of fish, and the negative effects of climate warming on growth are hypothesised to be more severe for larger fish.     

Water velocity shapes juvenile salmonids

Phenotypic plasticity in morphology is often considered adaptive. Stream-living fish encounter considerable spatial and temporal environmental variation in their native habitats, and the ability to adapt to this variation is of utmost importance. We studied experimentally whether water velocity affects the body shape of juvenile Atlantic salmon (Salmo salar m. sebago Girard) and brown trout (Salmo trutta m. lacustris L.). The fish were reared in slow and fast water flow, and their morphology was studied by measuring a number of morphometric characters. We studied which characters differed between the environments in each species, and found that water velocity caused morphological differentiation in both salmon and brown trout. The differences occurred especially in body height as well as in fin sizes, characters that are very likely to be of functional importance for life in the stream environment. Salmon in fast flow became more robust, whereas brown trout in fast flow became slightly more streamlined. The observed variation in body morphology of salmon and brown trout indicates phenotypic plasticity, but the species differed in their response to environmental variation, which may be due to different energetics and cost reduction strategies. Morphological differentiation caused by water flow occurred very rapidly, within 1-month exposure to the different water flows. This revised version was published online in November 2006 with corrections to the Cover Date.     

The foraging and antipredator behaviour of growth-enhanced transgenic Atlantic salmon

Growth rate has been established as a key parameter influencing foraging decisions involving the risk of predation. Through genetic manipulation, transgenic salmon bred to contain and transmit a growth hormone transgene are able to achieve growth rates significantly greater than those of unmanipulated salmon. Using such growth-enhanced transgenic Atlantic salmon, we directly tested the hypothesis that relative growth rates should be correlated with willingness to risk exposure to a predator. We used size-matched transgenic and control salmon in two experiments where these fish could either feed in safety, or in the presence of the predator. The first experiment constrained the predator behind a Plexiglas partition (no risk of mortality), the second required the fish to feed in the same compartment as the predator (a finite risk of mortality). During these experiments, transgenic salmon had rates of consumption that were approximately five times that of the control fish and rates of movement approximately double that of controls. Transgenic salmon also spent significantly more time feeding in the presence of the predator, and consumed absolutely more food at that location. When there was a real risk of mortality, control fish almost completely avoided the dangerous location. Transgenic fish continued to feed at this location, but at a reduced level. These data demonstrate that the growth enhancement associated with the transgenic manipulation increases the level of risk these fish are willing to incur while foraging. If the genetic manipulation necessary to increase growth rates is achievable through evolutionary change, these experiments suggest that growth rates of Atlantic salmon may be optimized by the risk of predation. Copyright 1999 The Association for the Study of Animal Behaviour.     

Cleaning up the biogeography of Labroides dimidiatus using phylogenetics and morphometrics

Cleaner fishes are some of the most conspicuous organisms on coral reefs due to their behaviour and prominent body pattern, consisting of a lateral stripe and blue/yellow colouration. All obligate cleaner fishes share this body stripe pattern, which is an important signal for attracting client fishes. However, variability in the cleaning signal of the cleaner fish Labroides dimidiatus has been documented across its range. Here, we investigate the geographic distribution of cleaner signal polymorphisms in L. dimidiatus and contrast this to phylogeographic variation in mitochondrial (mt) DNA. We used samples from 12 sites for genetic analyses, encompassing much of L. dimidiatus’ range from the Red Sea to Fiji. We obtained morphometric measures of the cleaner signal body stripe width from individuals among six of the sites and qualitatively grouped tail stripe shape. mtDNA control region sequences were used for phylogenetic and population genetic analyses. We found that body stripe width was significantly correlated with tail stripe shape and geographical location, with Indian Ocean populations differing in morphology from western Pacific populations. L. dimidiatus haplotypes formed two reciprocally monophyletic clades, although in contrast to morphology, Japanese cleaner fish fell within the same clade as Indian Ocean cleaner fish and both clade types were sympatric in Papua New Guinea. An additional novel finding of our research was that the inclusion of two closely related cleaner fish species, Labroides pectoralis and Labroides bicolor, in the phylogenetic analysis rendered L. dimidiatus polyphyletic. Overall, the findings suggest the diversity within L. dimidiatus is underestimated.     

Morphological divergence of North‐European nine‐spined sticklebacks (Pungitius pungitius): signatures of parallel evolution

Parallel evolution is characterised by repeated, independent occurrences of similar phenotypes in a given habitat type, in different parts of the species distribution area. We studied body shape and body armour divergence between five marine, four lake, and ten pond populations of nine‐spined sticklebacks [Pungitius pungitius (Linnaeus, 1758)] in Fennoscandia. We hypothesized that marine and lake populations (large water bodies, diverse fish fauna) would be similar, whereas sticklebacks in isolated ponds (small water bodies, simple fish fauna) would be divergent. We found that pond fish had deeper bodies, shorter caudal peduncles, and less body armour (viz. shorter/absent pelvic spines, reduced/absent pelvic girdle, and reduced number of lateral plates) than marine fish. Lake fish were intermediate, but more similar to marine than to pond fish. Results of our common garden experiment concurred with these patterns, suggesting a genetic basis for the observed divergence. We also found large variation among populations within habitat types, indicating that environmental variables other than those related to gross habitat characteristics might also influence nine‐spined stickleback morphology. Apart from suggesting parallel evolution of morphological characteristics of nine‐spined sticklebacks in different habitats, the results also show a number of similarities to the evolution of three‐spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) morphology. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 403–416.     

Environmental correlates of life-history variation in juvenile chinook salmon, Oncorhynchus tshawytscha (Walbaum)

Throughout its native North Pacific, the chinook salmon, Oncorhynchus tshawytscha (Walbaum), exists as twolife-history types that aredistinguished by the age at which juvenile salmon migrate to sea as smolts. 'Stream-type' chinook migrate seaward after I or more years of feeding in fresh water, whereas 'ocean-type' fish migrate to sea as newly emerged fry or after 2–3 months in fresh water. Stream-type chinook predominate in populations distant from the sea south of 56° N, and in both inland and coastal populations north of this point. By contrast, ocean-type chinook predominate in coastal populations south of 56° N, but are rare in populations in more northerly latitudes. Stream-type populations are associated with areas of low 'growth opportunity' (as measured by temperature and photoperiod regimes) and/or areas distant from the sea compared to ocean-type. Geographic variability in juvenile life history is suggested to result, in part, from environmental modulation of smolting timing via differences in growth opportunity among geo-graphic areas. In addition, differences in migration distance and temperature regime may result in selection for different sizes at migration among populations which, through differences in growth opportunity, might promote geographic variability in age at seaward migration.