Phenotypic integration of behavioural and physiological traits is related to variation in growth among stocks of Chinook salmon

The selection for a single organismal trait like growth in breeding programs of farmed aquaculture species can counterintuitively lead to lowered harvestable biomass. We outbred a domesticated aquaculture stock of Chinook salmon (Oncorhynchus tshawytscha (Walbaum in Artedi, 1792)) with seven wild stocks from British Columbia, Canada. We then examined how functionally related traits underlying energy management – diel variation in cortisol and foraging, social, and movement behaviours — predicted stock-level variation in growth during the freshwater life history stage, which is a performance metric under aquaculture selection. Outbreeding generated significant variation in diel cortisol secretion and behaviours across stocks, and these traits co-varied, suggesting tight integration despite hybridization. The coupling of nighttime cortisol exposure with the daytime behavioural phenotype was the strongest predictor of stock-level variation in body mass. Our results suggest that selection for an integrated phenotype rather than on a single mechanistic trait alone can generate the greatest effect on aquaculture fish growth under outbreeding practices. Furthermore, selecting for these traits at the stock level may increase efficiency of farming methods designed to consistently maximize fish performance on a large scale.

• Publication year

  2018

• Venue

  Canadian Journal of Fisheries and Aquatic Sciences

• Publication date

  2018-03-24

• Fields of study

  Biology, Environmental Science

• Identifiers
  DOI 10.1139/CJFAS-2017-0367
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar

• No claims are published for this paper.

• No concepts are published for this paper.

• Domestic-wild hybridization to improve aquaculture performance in Chinook salmon

  2019cited by this paper
• Coping styles in farmed fish: consequences for aquaculture

  2017cited by this paper
• state of world fisheries and aquaculture

  2017cited by this paper
• Future Protein Supply and Demand: Strategies and Factors Influencing a Sustainable Equilibrium

  2017cited by this paper
• Endocrine Flexibility: Optimizing Phenotypes in a Dynamic World?

  2016cited by this paper
• Population‐level responses of life history traits to flow regime in three common stream fish species

  2016cited by this paper
• Prenatal Stress Exposure Generates Higher Early Survival and Smaller Size without Impacting Developmental Rate in a Pacific Salmon.

  2016cited by this paper
• Fitness of multidimensional phenotypes in dynamic adaptive landscapes.

  2015cited by this paper
• Multigenerational outbreeding effects in Chinook salmon (Oncorhynchus tshawytscha)

  2014cited by this paper
• What determines growth potential and juvenile quality of farmed fish species

  2013influential reference
• An overview of the evolutionary causes and consequences of behavioural plasticity

  2013cited by this paper
• Environmental stressors alter relationships between physiology and behaviour.

  2013cited by this paper
• Can We Predict Personality in Fish? Searching for Consistency over Time and across Contexts

  2013cited by this paper
• Acute aluminium phosphide poisoning: Can we predict survival?

  2012cited by this paper
• The integrated phenotype.

  2012influential reference
• Smolt Physiology and Endocrinology

  2012cited by this paper
• Local adaptation in marine invertebrates.

  2011cited by this paper
• Future protein supply

  2011cited by this paper
• Environmental drivers of Atlantic salmon behaviour in sea-cages: A review

  2011cited by this paper
• Extent and scale of local adaptation in salmonid fishes: review and meta-analysis

  2011cited by this paper
• Conservation and enhancement of wild fish populations: preserving genetic quality versus

  2011cited by this paper
• Stress and fish reproduction: the roles of allostasis and hormesis.

  2010cited by this paper
• MATERNAL ADJUSTMENT OF EGG SIZE ORGANIZES ALTERNATIVE ESCAPE BEHAVIORS, PROMOTING ADAPTIVE PHENOTYPIC INTEGRATION

  2010cited by this paper
• Maternal adjustment of egg size organizes alternative escape behaviors, promoting adaptive phenotypic integration.

  2010cited by this paper
• Farming and the Fate of Wild Nature

  2009cited by this paper
• The Global Food Crisis

  2009cited by this paper
• Phenotypic integration and independence: Hormones, performance, and response to environmental change.

  2009influential reference
• Hormone-mediated suites as adaptations and evolutionary constraints

  2008cited by this paper
• A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change

  2008cited by this paper
• What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions

  2007cited by this paper
• Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort

  2007cited by this paper
• The effect of group composition on the welfare of African catfish (Clarias gariepinus)

  2006cited by this paper
• Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management

  2006cited by this paper
• Growth and Behavioral Consequences of Introgression of a Domesticated Aquaculture Genotype into a Native Strain of Coho Salmon

  2006cited by this paper
• The Integration of Behaviour into Comparative Physiology*

  2005cited by this paper
• REPRODUCTIVE ISOLATION CAUSED BY NATURAL SELECTION AGAINST IMMIGRANTS FROM DIVERGENT HABITATS

  2005cited by this paper
• Photoperiod affects growth, behaviour and stress variables in Clarias gariepinus

  2005cited by this paper
• Selection and breeding programs in aquaculture

  2005cited by this paper
• The alluring simplicity and complex reality of genetic rescue.

  2004cited by this paper
• Effects of cortisol on food intake, growth, and forebrain neuropeptide Y and corticotropin-releasing factor gene expression in goldfish.

  2004cited by this paper
• Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation

  2004cited by this paper
• Introduction to Conservation Genetics

  2003cited by this paper
• Phenotypic integration: studying the ecology and evolution of complex phenotypes

  2003cited by this paper
• Integrating stress physiology, environmental change, and behavior in free-living sparrows.

  2003cited by this paper
• Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change.

  2003cited by this paper
• Group size influences foraging effort independent of predation risk: an experimental study on rainbow trout

  2003cited by this paper
• Designing aquaculture mass selection programs to avoid high inbreeding rates

  2002cited by this paper
• Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids1

  2002cited by this paper
• Effects of cortisol on aggression and locomotor activity in rainbow trout.

  2002cited by this paper
• Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes

  2002cited by this paper
• The problems with hybrids: setting conservation guidelines

  2001cited by this paper
• Fish hatchery management.

  2001cited by this paper
• Stress hormones: good and bad.

  2000cited by this paper
• Seasonal and Diel Changes in Behaviour, Microhabitat use and Preferences by Young Pool-dwelling Atlantic Salmon, Salmo salar, and Brown Trout, Salmo trutta

  2000cited by this paper
• Local drift load and the heterosis of interconnected populations

  2000cited by this paper
• Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel's white-crowned sparrow.

  1999cited by this paper
• Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation

  1999cited by this paper
• The Effects of Chronic Plasma Cortisol Elevation on the Feeding Behaviour, Growth, Competitive Ability, and Swimming Performance of Juvenile Rainbow Trout

  1999cited by this paper
• The effect of photoperiod on diel rhythms in serum melatonin, cortisol, glucose, and electrolytes in the common dentex, Dentex dentex.

  1999cited by this paper
• Regulation of nutrient intake and energy balance in salmon

  1999cited by this paper
• HETEROSIS AND OUTBREEDING DEPRESSION IN INTERPOPULATION CROSSES SPANNING A WIDE RANGE OF DIVERGENCE

  1999cited by this paper
• MATERNAL EFFECTS ON OFFSPRING SIZE: VARIATION THROUGH EARLY DEVELOPMENT OF CHINOOK SALMON

  1999cited by this paper
• Outbreeding depression in hybrids between odd- and even-broodyear pink salmon

  1999cited by this paper
• Costs and limits of phenotypic plasticity.

  1998cited by this paper
• Nocturnal activity of juvenile Atlantic salmon (Salmo salar) in late summer: evidence of diel activity partitioning

  1997cited by this paper
• The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon

  1997cited by this paper
• Effects of inbreeding on growth and reproductive traits in rainbow trout (Oncorhynchus mykiss)

  1996cited by this paper
• Vertical distribution of Atlantic salmon (Salmo solar L.) in net pens: trade-off between surface light avoidance and food attraction

  1995cited by this paper
• Vertical distribution of Atlantic salmon (Salmo salar) as a function of illumination

  1993cited by this paper
• Feast and famine: critical role of glucocorticoids with insulin in daily energy flow.

  1993cited by this paper
• Testing Assumptions of Fish Bioenergetics Models by Direct Estimation of Growth, Consumption, and Activity Rates

  1993cited by this paper
• Diel and Seasonal Changes in Resting Levels of Various Blood Parameters in Brook Trout (Salvelinus fontinalis)

  1992cited by this paper
• Group foraging versus solitary foraging efficiency in piscivorous predators: the perch, Perca fluviatilis, and pike, Esox lucius, patterns

  1992cited by this paper
• Interactions of corticosterone with feeding, activity and metabolism in passerine birds

  1992cited by this paper
• A review of local adaptation in Salmonidac, with particular reference to Pacific and Atlantic salmon

  1991cited by this paper
• Pacific Salmon, Oncorhynchus spp., and the Definition of "Species" Under the Endangered Species Act

  1991cited by this paper
• Phenotypic Integration and Environmental ChangeWhat are the consequences of differential phenotypic plasticity of traits

  1989cited by this paper
• A multiple approach to behaviour studies of salmon reared in marine net pens

  1988cited by this paper
• Diel and seasonal changes in resting plasma cortisol levels in juvenile Atlantic salmon, Salmo salar L.

  1987cited by this paper
• Inbreeding in fish populations used for aquaculture

  1983cited by this paper
• Seasonal and diel changes in plasma cortisol levels of the brown trout, Salmo trutta L.

  1983cited by this paper
• Animal Physiology: Adaptation and Environment

  1975cited by this paper

• Genetic architecture and correlations between the gut microbiome and gut gene transcription in Chinook salmon (Oncorhynchus tshawytscha)

  2024cites this paper
• Exploiting animal personality to reduce chronic stress in captive fish populations

  2022cites this paper
• Single generation exposure to a captive diet: a primer for domestication selection in a salmonid fish?

  2020cites this paper
• Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels

  2020cites this paper
• Transgenerational effects of chronic environmental stress

  2020cites this paper
• Rearing conditions differentially affect behavioural phenotypes of male “jack” and “hooknose” Chinook salmon and their sisters in both fresh and salt water

  2020cites this paper
• Mimicking Transgenerational Signals of Future Stress: Thermal Tolerance of Juvenile Chinook Salmon Is More Sensitive to Elevated Rearing Temperature Than Exogenously Increased Egg Cortisol

  2020influential citation
• The effects of variation in acclimation- and growth-maximizing behavioural types of outcrossed Chinook salmon (Oncorhynchus tshawytscha) on growth and survival in captivity

  2019cites this paper
• Life in captivity: varied behavioural responses to novel setting and food types in first-generation hybrids of farmed and wild juvenile Chinook salmon (Oncorhynchus tshawytscha)

  2019cites this paper
• Prenatal stress as a potential adaptive modulator of offspring survival, phenotype, and performance in response to elevated temperatures

  2019cites this paper