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Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals.
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Metabolismo Basal , Animais , Humanos , FenótipoRESUMO
Fisheries induce one of the strongest anthropogenic selective pressures on natural populations, but the genetic effects of fishing remain unclear. Crucially, we lack knowledge of how capture-associated selection and its interaction with reductions in population density caused by fishing can potentially shift which genes are under selection. Using experimental fish reared at two densities and repeatedly harvested by simulated trawling, we show consistent phenotypic selection on growth, metabolism, and social behavior regardless of density. However, the specific genes under selection-mainly related to brain function and neurogenesis-varied with the population density. This interaction between direct fishing selection and density could fundamentally alter the genomic responses to harvest. The evolutionary consequences of fishing are therefore likely context dependent, possibly varying as exploited populations decline. These results highlight the need to consider environmental factors when predicting effects of human-induced selection and evolution.
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Pesqueiros , Características de História de Vida , Seleção Genética , Agressão , Animais , Metabolismo Energético/genética , Feminino , Estudos de Associação Genética , Genoma , Masculino , Fenótipo , Densidade Demográfica , Peixe-ZebraRESUMO
The costs and benefits of being social vary with environmental conditions, so individuals must weigh the balance between these trade-offs in response to changes in the environment. Temperature is a salient environmental factor that may play a key role in altering the costs and benefits of sociality through its effects on food availability, predator abundance, and other ecological parameters. In ectotherms, changes in temperature also have direct effects on physiological traits linked to social behaviour, such as metabolic rate and locomotor performance. In light of climate change, it is therefore important to understand the potential effects of temperature on sociality. Here, we took the advantage of a 'natural experiment' of threespine sticklebacks from contrasting thermal environments in Iceland: geothermally warmed water bodies (warm habitats) and adjacent ambient-temperature water bodies (cold habitats) that were either linked (sympatric) or physically distinct (allopatric). We first measured the sociability of wild-caught adult fish from warm and cold habitats after acclimation to a low and a high temperature. At both acclimation temperatures, fish from the allopatric warm habitat were less social than those from the allopatric cold habitat, whereas fish from sympatric warm and cold habitats showed no differences in sociability. To determine whether differences in sociability between thermal habitats in the allopatric population were heritable, we used a common garden breeding design where individuals from the warm and the cold habitat were reared at a low or high temperature for two generations. We found that sociability was indeed heritable but also influenced by rearing temperature, suggesting that thermal conditions during early life can play an important role in influencing social behaviour in adulthood. By providing the first evidence for a causal effect of rearing temperature on social behaviour, our study provides novel insights into how a warming world may influence sociality in animal populations.
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Smegmamorpha , Animais , Aclimatação , Temperatura , Peixes/fisiologia , ÁguaRESUMO
European sea bass (Dicentrarchus labrax) is a large, economically important fish species with a long generation time whose long-term resilience to ocean acidification (OA) and warming (OW) is not clear. We incubated sea bass from Brittany (France) for two generations (>5â years in total) under ambient and predicted OA conditions (PCO2: 650 and 1700â µatm) crossed with ambient and predicted OW conditions in F1 (temperature: 15-18°C and 20-23°C) to investigate the effects of climate change on larval and juvenile growth and metabolic rate. We found that in F1, OA as a single stressor at ambient temperature did not affect larval or juvenile growth and OW increased developmental time and growth rate, but OAW decreased larval size at metamorphosis. Larval routine and juvenile standard metabolic rate were significantly lower in cold compared with warm conditioned fish and also lower in F0 compared with F1 fish. We did not find any effect of OA as a single stressor on metabolic rate. Juvenile PO2,crit was not affected by OA or OAW in both generations. We discuss the potential underlying mechanisms resulting in the resilience of F0 and F1 larvae and juveniles to OA and in the beneficial effects of OW on F1 larval growth and metabolic rate, but contrastingly in the vulnerability of F1, but not F0 larvae to OAW. With regard to the ecological perspective, we conclude that recruitment of larvae and early juveniles to nursery areas might decrease under OAW conditions but individuals reaching juvenile phase might benefit from increased performance at higher temperatures.
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Bass , Animais , Bass/metabolismo , Concentração de Íons de Hidrogênio , Larva , Oceanos e Mares , Água do Mar , TemperaturaRESUMO
Interest in the measurement of metabolic rates is growing rapidly, because of the importance of metabolism in advancing our understanding of organismal physiology, behaviour, evolution and responses to environmental change. The study of metabolism in aquatic animals is undergoing an especially pronounced expansion, with more researchers utilising intermittent-flow respirometry as a research tool than ever before. Aquatic respirometry measures the rate of oxygen uptake as a proxy for metabolic rate, and the intermittent-flow technique has numerous strengths for use with aquatic animals, allowing metabolic rate to be repeatedly estimated on individual animals over several hours or days and during exposure to various conditions or stimuli. There are, however, no published guidelines for the reporting of methodological details when using this method. Here, we provide the first guidelines for reporting intermittent-flow respirometry methods, in the form of a checklist of criteria that we consider to be the minimum required for the interpretation, evaluation and replication of experiments using intermittent-flow respirometry. Furthermore, using a survey of the existing literature, we show that there has been incomplete and inconsistent reporting of methods for intermittent-flow respirometry over the past few decades. Use of the provided checklist of required criteria by researchers when publishing their work should increase consistency of the reporting of methods for studies that use intermittent-flow respirometry. With the steep increase in studies using intermittent-flow respirometry, now is the ideal time to standardise reporting of methods, so that - in the future - data can be properly assessed by other scientists and conservationists.
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Consumo de Oxigênio , Oxigênio , Animais , Metabolismo Basal , TemperaturaRESUMO
Transgenerational inheritance from both parental lines can occur by genetic and epigenetic inheritance. Maternal effects substantially influence offspring survival and fitness. However, investigation of the paternal contribution to offspring success has been somewhat neglected. In the present study, adult zebrafish were separated into female and male groups exposed for 21 days to either a control diet or to a diet containing water accommodated fractions of crude oil. Four F1 offspring groups were obtained: (1) control (non-exposed parents), (2) paternally exposed, (3) maternally exposed and (4) dual-parent-exposed. To determine the maternal and paternal influence on their offspring, we evaluated responses from molecular to whole organismal levels in both generations. Growth rate, hypoxia resistance and heart rate did not differ among parental groups. However, global DNA methylation in heart tissue was decreased in oil-exposed fish compared with control parents. This decrease was accompanied by an upregulation of glycine N-methyltransferase. Unexpectedly, maternal, paternal and dual exposure all enhanced survival of F1 offspring raised in oiled conditions. Regardless of parental exposure, however, F1 offspring exposed to oil exhibited bradycardia. Compared with offspring from control parents, global DNA methylation was decreased in the three offspring groups derived from oil-exposed parents. However, no difference between groups was observed in gene regulation involved in methylation transfer, suggesting that the changes observed in the F1 populations may have been inherited from both parental lines. Phenotypic responses during exposure to persistent environmental stressors in F1 offspring appear to be influenced by maternal and paternal exposure, potentially benefitting offspring populations to survive in challenging environments.
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Hereditariedade , Petróleo , Animais , Epigênese Genética , Feminino , Humanos , Masculino , Exposição Paterna/efeitos adversos , Peixe-Zebra/genéticaRESUMO
While evidence suggests that warming may impact cognition of ectotherms, the underlying mechanisms remain poorly understood. A possible but rarely considered mechanism is that the metabolic response of ectotherms to warming is associated with changes in brain morphology and function. Here, we compared aerobic metabolism, brain volume, boldness and accuracy of maze solving of common minnows (Phoxinus phoxinus) acclimated for 8 months to either their current optimal natural (14°C) or warm (20°C) water temperature. Metabolic rates indicated increased energy expenditure in warm-acclimated fish, but also at least partial thermal compensation as warm-acclimated fish maintained high aerobic scope. Warm-acclimated fish had larger brains than cool-acclimated fish. The volume of the dorsal medulla relative to the overall brain size was larger in warm- than in cool-acclimated fish, but the proportion of other brain regions did not differ between the temperature treatments. Warm-acclimated fish did not differ in boldness but made more errors than cool-acclimated fish in exploring the maze across four trials. Inter-individual differences in the number of exploration errors were repeatable across the four trials of the maze test. Our findings suggest that in warm environments, maintaining a high aerobic scope, which is important for the performance of physically demanding tasks, can come at the cost of changes in brain morphology and impairment of the capacity to explore novel environments. This trade-off could have strong fitness implications for wild ectotherms.
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Aclimatação , Cyprinidae , Animais , Encéfalo , Temperatura Baixa , TemperaturaRESUMO
Increased ocean temperatures are causing mass bleaching of anemones and corals in the tropics worldwide. While such heat-induced loss of algal symbionts (zooxanthellae) directly affects anemones and corals physiologically, this damage may also cascade on to other animal symbionts. Metabolic rate is an integrative physiological trait shown to relate to various aspects of organismal performance, behaviour and locomotor capacity, and also shows plasticity during exposure to acute and chronic stressors. As climate warming is expected to affect the physiology, behaviour and life history of animals, including ectotherms such as fish, we measured if residing in bleached versus unbleached sea anemones (Heteractis magnifica) affected the standard (i.e. baseline) metabolic rate and behaviour (activity) of juvenile orange-fin anemonefish (Amphiprion chrysopterus). Metabolic rate was estimated from rates of oxygen uptake [Formula: see text], and the standard metabolic rate [Formula: see text] of anemonefish from bleached anemones was significantly higher by 8.2% compared with that of fish residing in unbleached anemones, possibly due to increased stress levels. Activity levels did not differ between fish from bleached and unbleached anemones. As [Formula: see text] reflects the minimum cost of living, the increased metabolic demands may contribute to the negative impacts of bleaching on important anemonefish life history and fitness traits observed previously (e.g. reduced spawning frequency and lower fecundity).
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Perciformes/metabolismo , Anêmonas-do-Mar/fisiologia , Simbiose/fisiologia , Animais , Mudança Climática , Locomoção/fisiologia , Consumo de Oxigênio/fisiologia , Perciformes/fisiologiaRESUMO
Morphological variation is the outward manifestation of development and provides fodder for adaptive evolution. Because of this contingency, evolution is often thought to be biased by developmental processes and functional interactions among structures, which are statistically detectable through forms of covariance among traits. This can take the form of substructures of integrated traits, termed modules, which together comprise patterns of variational modularity. While modularity is essential to an understanding of evolutionary potential, biologists currently have little understanding of its genetic basis and its temporal dynamics over generations. To address these open questions, we compared patterns of craniofacial modularity among laboratory strains, defined mutant lines and a wild population of zebrafish (Danio rerio). Our findings suggest that relatively simple genetic changes can have profound effects on covariance, without greatly affecting craniofacial shape. Moreover, we show that instead of completely deconstructing the covariance structure among sets of traits, mutations cause shifts among seemingly latent patterns of modularity suggesting that the skull may be predisposed towards a limited number of phenotypes. This new insight may serve to greatly increase the evolvability of a population by providing a range of 'preset' patterns of modularity that can appear readily and allow for rapid evolution.
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Evolução Biológica , Fenótipo , Crânio/anatomia & histologia , Peixe-Zebra/anatomia & histologia , Peixe-Zebra/genética , Animais , Variação Genética , MutaçãoRESUMO
As selection acts on multivariate phenotypes, the evolution of traits within populations not only depends on the genetic basis of each trait, but also on the genetic relationships among traits. As metabolic rate is often related to vital traits such as growth, physiology and behaviour, its variation and evolution is expected to have important repercussions on individual fitness. However, the majority of the correlations between metabolic rate and other traits has been based on phenotypic correlations, while genetic correlations, basis for indirect selection and evolution, have been overlooked. Using a case study, we explore the importance of properly estimating genetic correlations to understand and predict evolution of multivariate phenotypes. We show that selection on metabolic traits could result in indirect selection mainly on growth-related traits, owing to strong genetic correlations, but not on swimming or risk-taking and sociability behaviour even if they covary phenotypically. While phenotypic correlation can inform about genetic correlation direction, caution is needed in predicting the magnitude of genetic correlation. Therefore, even though phenotypic correlations among physiological and behavioural traits could be useful, deriving evolutionary conclusions based purely on them is not robust. In short, proper estimation of genetic correlations is needed when predicting evolutionary consequences. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.
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Natação , Fenótipo , Metabolismo Energético/fisiologiaRESUMO
Understanding the critical thresholds of dissolved oxygen (O2) that trigger adaptive physiological responses in aquatic organisms is long hampered by a lack of robust, non-lethal or non-invasive methodologies. The isotope fractionation of triple O2 isotopes (18O/17O/16O) during respiration is linked to the amount of oxygen utilised, offering a potential avenue for new insights. Our experimental research involved measuring the oxygen isotope fractionation of dissolved O2 in closed-system aquatic respirometry experiments with wild sticklebacks (Gasterosteus aculeatus). These fish were either naturally adapted or experimentally acclimated to hypoxic and normoxic conditions. The aim was to observe their oxygen usage and isotope fractionation in response to increasingly severe hypoxia. Initial observations revealed a progressive 18O enrichment from the preferential uptake of 16O to a dissolved oxygen threshold of 3-5 mg O2 L-1, followed by an apparent reversal in oxygen isotope fractionation, which is mixing of 16O and 17O with the remaining O2 pool across all populations and indicative of a systematic change in oxygen metabolism among the fish. Unexpectedly, sticklebacks adapted to hypoxia but acclimated to normoxia exhibited stronger oxygen isotope fractionation compared to those adapted to normoxia and acclimated to hypoxia, contradicting the hypothesis that hypoxia adaptation would lead to reduced isotope discrimination due to more efficient oxygen uptake. These preliminary experimental results highlight the novel potential of using dissolved O2 isotopes as a non-invasive, non-lethal method to quantitatively assess metabolic thresholds in aquatic organisms. This approach could significantly improve our understanding of the critical oxygen responses and adaptation mechanisms in fish and other aquatic organisms across different oxygen environments, marking a significant step forward in aquatic ecological and physiological research.
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The epigenome is the suite of interacting chemical marks and molecules that helps to shape patterns of development, phenotypic plasticity and gene regulation, in part due to its responsiveness to environmental stimuli. There is increasing interest in understanding the functional and evolutionary importance of this sensitivity under ecologically realistic conditions. Observations that epigenetic variation abounds in natural populations have prompted speculation that it may facilitate evolutionary responses to rapid environmental perturbations, such as those occurring under climate change. A frequent point of contention is whether epigenetic variants reflect genetic variation or are independent of it. The genome and epigenome often appear tightly linked and interdependent. While many epigenetic changes are genetically determined, the converse is also true, with DNA sequence changes influenced by the presence of epigenetic marks. Understanding how the epigenome, genome and environment interact with one another is therefore an essential step in explaining the broader evolutionary consequences of epigenomic variation. Drawing on results from experimental and comparative studies carried out in diverse plant and animal species, we synthesize our current understanding of how these factors interact to shape phenotypic variation in natural populations, with a focus on identifying similarities and differences between taxonomic groups. We describe the main components of the epigenome and how they vary within and between taxa. We review how variation in the epigenome interacts with genetic features and environmental determinants, with a focus on the role of transposable elements (TEs) in integrating the epigenome, genome and environment. And we look at recent studies investigating the functional and evolutionary consequences of these interactions. Although epigenetic differentiation in nature is likely often a result of drift or selection on stochastic epimutations, there is growing evidence that a significant fraction of it can be stably inherited and could therefore contribute to evolution independently of genetic change.
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Investigating the nature of physiological traits potentially related to fitness is important towards a better understanding of how species and/or populations may respond to selective pressures imposed by contrasting environments. In northern species in particular, the ability to mobilize energy reserves to compensate for the low external energy intake during winter is crucial. However, the phenotypic and genetic bases of energy reserve accumulation and mobilization have rarely been investigated, especially pertaining to variation in strategy adopted by different populations. In the present study, we documented variation in several energy reserve variables and estimated their quantitative genetic basis to test the null hypothesis of no difference in variation at those traits among three strains of brook charr (Salvelinus fontinalis) and their reciprocal hybrids. Our results indicate that the strategy of winter energy preparation and mobilization was specific to each strain, whereby (1) domestic fish accumulated a higher amount of energy reserves before winter and kept accumulating liver glycogen during winter despite lower feeding; (2) Laval fish used liver glycogen and lipids during winter and experienced a significant decrease in condition factor; (3) Rupert fish had relatively little energy reserves accumulated at the end of fall and preferentially mobilized visceral fat during winter. Significant heritability for traits related to the accumulation and use of energy reserves was found in the domestic and Laval but not in the Rupert strain. Genetic and phenotypic correlations also varied among strains, which suggested population-specific genetic architecture underlying the expression of these traits. Hybrids showed limited evidence of non-additive effects. Overall, this study provides the first evidence of a genetically based-and likely adaptive-population-specific strategy for energy mobilization related to overwinter survival.
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Variação Genética , Estações do Ano , Truta/genética , Adaptação Fisiológica/genética , Animais , Quimera/genética , Ecossistema , Metabolismo Energético/genética , Genótipo , Metabolismo dos Lipídeos/genética , Glicogênio Hepático/metabolismo , População/genética , Truta/metabolismoRESUMO
Dietary crude oil exposure has detrimental morpho-physiological effects in fishes, including endocrine disruption. However, little is known about how it influences sex differentiation and its potential for skewing sex ratios of populations. Appropriate sex ratio is important for maintaining effective population size and structure. Deviations of these ratios can compromise population growth and maintenance and may induce changes in a species' evolutionary trajectory. We assessed the potential of dietary exposure to crude oil (6.5, 11.4, and 17.5 mg/kg food) to alter sex differentiation in the zebrafish (Danio rerio) (20-35 days post fertilization (dpf)) and subsequently skew the adult (90 dpf) sex ratio. Multiple health- and fitness-related phenotypic traits (i.e., body mass and length, condition factor, heart rate, oxygen consumption, and their capacity to cope with hypoxia) were also assessed to better understand the effects of dietary crude oil exposure. We showed that dietary exposure to crude oil during the process of sex differentiation skewed sex ratio towards males (up to 0.34:1 female to male ratio in the highest oil concentration). Remarkably, this effect occurred independently of affecting physiological variables and female gonad characteristics, thus highlighting just how subtle the effects of dietary crude oil exposure can be. Our results suggest that, although fish were in an apparently healthy state during experimentation, sex ratio was still impacted, potentially compromising the resilience of the population. Therefore, considering how complex chemical mixtures affect organisms at several levels (molecular-individual) in experimental designs is warranted to better understand the implications of the exposures and the hazards that populations face in the wild.
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Petróleo , Poluentes Químicos da Água , Animais , Feminino , Masculino , Diferenciação Sexual , Peixe-Zebra/fisiologia , Razão de Masculinidade , Exposição Dietética , Petróleo/toxicidade , Poluentes Químicos da Água/toxicidadeRESUMO
Fish red blood cells contain nucleus and therefore carry on active transcription throughout their life. As the steady state level of mRNA depends both on the production and breakdown of the mRNA, it is important to pay attention to sampling, cell separation, mRNA extraction, and transcript stability to conduct a comprehensive erythrocyte genomics study. In addition, particular attention should be made to tie the transcriptional changes to corresponding protein activities, as only those would impact cellular functions. Here, we thus describe the different steps to conduct comprehensive functional genomics studies with fish erythrocytes.
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Eritrócitos , Peixes , Animais , Eritrócitos/metabolismo , Peixes/genética , Genômica , RNA Mensageiro/genética , RNA Mensageiro/metabolismoRESUMO
Fishing-associated selection is one of the most important human-induced evolutionary pressures for natural populations. However, it is unclear whether fishing leads to heritable phenotypic changes in the targeted populations, as the heritability and genetic correlations of traits potentially under selection have received little attention. In addition, phenotypic changes could arise from fishing-associated environmental effects, such as reductions in population density. Using fish reared at baseline and reduced group density and repeatedly harvested by simulated trawling, we show that trawling can induce direct selection on fish social behaviour. As sociability has significant heritability and is also genetically correlated with activity and exploration, trawling has the potential to induce both direct selection and indirect selection on a variety of fish behaviours, potentially leading to evolution over time. However, while trawling selection was consistent between density conditions, the heritability and genetic correlations of behaviours changed according to the population density. Fishing-associated environmental effects can thus modify the evolutionary potential of fish behaviour, revealing the need to use a more integrative approach to address the evolutionary consequences of fishing.
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In aquatic ecology, studies have commonly employed a tagging technique known as visible implant elastomer (VIE). This method has not been widely adopted by the zebrafish research community and also lacks refinement with regard to animal welfare. The current paper introduces a new VIE tagging protocol, with the aim of improving existing tagging techniques by placing particular emphasis on the Three Rs. To improve animal welfare and fish survival, we added the use of an analgesic compound (lidocaine) through the marking procedure, followed by after-treatment with antiseptics (melaleuca, aloe vera, and PVP-I as active ingredients) to improve tissue regeneration and healing. The newly improved protocol has been quantitatively evaluated on different populations and age groups of zebrafish. This study will be useful to the scientific zebrafish community and to the wider field including biologist and aquarists, especially in consideration of animal welfare, where tagging techniques are considered as a potential noxious stimulus for fish.
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[This corrects the article DOI: 10.1093/database/coz082.].
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Lay summary Selective harvest of wild organisms by humans can influence the evolution of plants and animals, and fishing is recognized as a particularly strong driver of this process. Importantly, these effects occur alongside environmental change. Here we show that aquatic hypoxia can alter which individuals within a fish population are vulnerable to capture by trawling, potentially altering the selection and evolutionary effects stemming from commercial fisheries.
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There is increasing evidence that intense fishing pressure is not only depleting fish stocks but also causing evolutionary changes to fish populations. In particular, body size and fecundity in wild fish populations may be altered in response to the high and often size-selective mortality exerted by fisheries. While these effects can have serious consequences for the viability of fish populations, there are also a range of traits not directly related to body size which could also affect susceptibility to capture by fishing gears-and therefore fisheries-induced evolution (FIE)-but which have to date been ignored. For example, overlooked within the context of FIE is the likelihood that variation in physiological traits could make some individuals within species more vulnerable to capture. Specifically, traits related to energy balance (e.g., metabolic rate), swimming performance (e.g., aerobic scope), neuroendocrinology (e.g., stress responsiveness) and sensory physiology (e.g., visual acuity) are especially likely to influence vulnerability to capture through a variety of mechanisms. Selection on these traits could produce major shifts in the physiological traits within populations in response to fishing pressure that are yet to be considered but which could influence population resource requirements, resilience, species' distributions and responses to environmental change.