Evolutionary relationships between metabolism and behaviour require genetic correlations.

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'.

Differential metabolic responses in bold and shy sea anemones during a simulated heatwave.

As climate change-induced heatwaves become more common, phenotypic plasticity at multiple levels is a key mitigation strategy by which organisms can optimise selective outcomes. In ectotherms, changes to both metabolism and behaviour can help alleviate thermal stress. Nonetheless, no study in any ectotherm has yet empirically investigated how changing temperatures affect among-individual differences in the associations between these traits. Using the beadlet anemone (Actinia equina), an intertidal species from a thermally heterogeneous environment, we investigated how individual metabolic rates, linked to morphotypic differences in A. equina, and boldness were related across changing temperatures. A crossed-over design and a temporal control were used to test the same individuals at a non-stressful temperature, 13°C, and under a simulated heatwave at 21°C. At each temperature, short-term repeated measurements of routine metabolic rate (RMR) and a single measurement of a repeatable boldness-related behaviour, immersion response time (IRT), were made. Individual differences, but not morphotypic differences, were highly predictive of metabolic plasticity, and the plasticity of RMR was associated with IRT. At 13°C, shy animals had the highest metabolic rates, while at 21°C, this relationship was reversed. Individuals that were bold at 13°C also exhibited the highest metabolic rates at 21°C. Additional metabolic challenges during heatwaves could be detrimental to fitness in bold individuals. Equally, lower metabolic rates at non-stressful temperatures could be necessary for optimal survival as heatwaves become more common. These results provide novel insight into the relationship between metabolic and behavioural plasticity, and its adaptive implications in a changing climate.

Capture and discard practises associated with an ornamental fishery affect the metabolic rate and aerobic capacity of three-striped dwarf cichlids Apistogramma trifasciata.

Fishing causes direct removal of individuals from wild populations but can also cause a physiological disturbance in fish that are released or discarded after capture. While sublethal physiological effects of fish capture have been well studied in commercial and recreational fisheries, this issue has been overlooked for the ornamental fish trade, where it is common to capture fish from the wild and discard non-target species. We examined metabolic responses to capture and discard procedures in the three-striped dwarf cichlid Apistogramma trifasciata, a popular Amazonian aquarium species that nonetheless may be discarded when not a target species. Individuals (n = 34) were tagged and exposed to each of four treatments designed to simulate procedures during the capture and discard process: 1) a non-handling control; 2) netting; 3) netting +30 seconds of air exposure; and 4) netting +60 seconds of air exposure. Metabolic rates were estimated using intermittent-flow respirometry, immediately following each treatment then throughout recovery overnight. Increasing amounts of netting and air exposure caused an acute increase in oxygen uptake and decrease in available aerobic scope. In general, recovery occurred quickly, with rapid decreases in oxygen uptake within the first 30 minutes post-handling. Notably, however, male fish exposed to netting +60 seconds of air exposure showed a delayed response whereby available aerobic scope was constrained <75% of maximum until ~4-6 hours post-stress. Larger fish showed a greater initial increase in oxygen uptake post-stress and slower rates of recovery. The results suggest that in the period following discard, this species may experience a reduced aerobic capacity for additional behavioural/physiological responses including feeding, territory defence and predator avoidance. These results are among the first to examine impacts of discard practises in the ornamental fishery and suggest ecophysiological research can provide valuable insight towards increasing sustainable practises in this global trade.

Colonization, diversity, and seasonality of fishes at pelagic fish aggregating devices.

The pelagic zone of the ocean can be a challenging environment in which to conduct research and as a result we lack the robust baseline abundance and diversity data, compared to what is available in more accessible coastal habitats, to be able to track changes or stressors to the biota in this environment. Many large-scale fisheries target pelagic fish, and much of the information available on these species is based on fisheries-dependent data that may be biased towards hotspots and commercially valuable fishes. Here, a long-term video and visual fish survey was conducted on two subsurface moored fish aggregating devices (FADs) in the pelagic waters of the central Bahamas to determine the feasibility of using moored pelagic FADs as tools for collecting fish abundance and diversity data. A wide range of species was documented, including large migratory fish that are the focus of commercial and recreational fisheries, and smaller often overlooked species on which little abundance or seasonality information exists. We found that FADs colonize quickly and reach a peak stable (albeit seasonally cyclical) abundance and diversity within the first several months after deployment. Species richness was higher in video surveys, but abundance was higher in visual surveys, except for sharks. Our results highlight the need to tailor survey methods to fit the context and study objective, and provide further evidence for the importance of fisheries-independent data in monitoring pelagic species.

Maze design: size and number of choices impact fish performance in cognitive assays.

Although studies on fish cognition are increasing, consideration of how methodological details influence the ability to detect and measure performance is lagging. Here, in two separate experiments the authors compared latency to leave the start position, latency to make a decision, levels of participation and success rates (whether fish entered the rewarded chamber as first choice) across different physical designs. Experiments compared fish performance across (a) two sizes of T-mazes, large and standard, and a plus-maze, and (b) open choice arenas with either two or four doors. Fish in T-mazes with longer arms took longer to leave the start chamber and were less likely to participate in a trial than fish in T-mazes with shorter arms. The number of options, or complexity, in a maze significantly impacted success but did not necessarily impact behavioural measures, and did not impact the number of fish that reached a chamber. Fish in the plus-maze had similar latencies to leave the start box and time to reach any chamber as fish in the same-sized T-maze but exhibited lower overall success. Similarly, in an open choice arena, increasing the number of options - doors to potential reward chambers - resulted in lower probability of success. There was an influence of reward position in the choice arena, with rewarded chambers closest to the sides of the arena resulting in lower latencies to enter and higher probability of decision success. Together the results allow the authors to offer practical suggestions towards optimal maze design for studies of fish cognition.

Temperature change effects on marine fish range shifts: A meta-analysis of ecological and methodological predictors.

The current effects of global warming on marine ecosystems are predicted to increase, with species responding by changing their spatial distributions. Marine ectotherms such as fish experience elevated distribution shifts, as temperature plays a key role in physiological functions and delineating population ranges through thermal constraints. Distributional response predictions necessary for population management have been complicated by high heterogeneity in magnitude and direction of movements, which may be explained by both biological as well as methodological study differences. To date, however, there has been no comprehensive synthesis of the interacting ecological factors influencing fish distributions in response to climate change and the confounding methodological factors that can affect their estimation. In this study we analyzed published studies meeting criteria of reporting range shift responses to global warming in 115 taxa spanning all major oceanic regions, totaling 595 three-dimensional population responses (latitudinal, longitudinal, and depth), with temperature identified as a significant driver. We found that latitudinal shifts were the fastest in non-exploited, tropical populations, and inversely correlated with depth shifts which, in turn, dominated at the trailing edges of population ranges. While poleward responses increased with rate of temperature change and latitude, niche was a key factor in predicting both depth (18% of variation) and latitudinal responses (13%), with methodological predictors explaining between 10% and 28% of the observed variance in marine fish responses to temperature change. Finally, we found strong geographical publication bias and limited taxonomical scope, highlighting the need for more representative and standardized research in order to address heterogeneity in distribution responses and improve predictions in face of changing climate.

Solving the conundrum of intra-specific variation in metabolic rate: A multidisciplinary conceptual and methodological toolkit: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species.

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.

Does aerobic scope influence geographical distribution of teleost fishes?

Many abiotic and biotic factors are known to shape species' distributions, but we lack understanding of how innate physiological traits, such as aerobic scope (AS), may influence the latitudinal range of species. Based on theoretical assumptions, a positive link between AS and distribution range has been proposed, but there has been no broad comparative study across species to test this hypothesis. We collected metabolic rate data from the literature and performed a phylogenetically informed analysis to investigate the influence of AS on the current geographical distributions of 111 teleost fish species. Contrary to expectations, we found a negative relationship between absolute latitude range and thermal peak AS in temperate fishes. We found no evidence for an association between thermal range of AS and the range of latitudes occupied for 32 species. Our main results therefore contradict the prevailing theory of a positive link between AS and distribution range in fish.

Geothermal stickleback populations prefer cool water despite multigenerational exposure to a warm environment.

Given the threat of climate change to biodiversity, a growing number of studies are investigating the potential for organisms to adapt to rising temperatures. Earlier work has predicted that physiological adaptation to climate change will be accompanied by a shift in temperature preferences, but empirical evidence for this is lacking. Here, we test whether exposure to different thermal environments has led to changes in preferred temperatures in the wild. Our study takes advantage of a "natural experiment" in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity year-round (warm habitats), adjacent to populations in ambient-temperature lakes (cold habitats). We used a shuttle-box approach to measure temperature preferences of wild-caught sticklebacks from three warm-cold population pairs. Our prediction was that fish from warm habitats would prefer higher water temperatures than those from cold habitats. We found no support for this, as fish from both warm and cold habitats had an average preferred temperature of 13°C. Thus, our results challenge the assumption that there will be a shift in ectotherm temperature preferences in response to climate change. In addition, since warm-habitat fish can persist at relatively high temperatures despite a lower-temperature preference, we suggest that preferred temperature alone may be a poor indicator of a population's adaptive potential to a novel thermal environment.

Testing the predictability of morphological evolution in contrasting thermal environments.

Gaining the ability to predict population responses to climate change is a pressing concern. Using a "natural experiment," we show that testing for divergent evolution in wild populations from contrasting thermal environments provides a powerful approach, and likely an enhanced predictive power for responses to climate change. Specifically, we used a unique study system in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity, adjacent to populations in ambient-temperature water. We focused on morphological traits across six pairs from warm and cold habitats. We found that fish from warm habitats tended to have a deeper mid-body, a subterminally orientated jaw, steeper craniofacial profile, and deeper caudal region relative to fish from cold habitats. Our common garden experiment showed that most of these differences were heritable. Population age did not appear to influence the magnitude or type of thermal divergence, but similar types of divergence between thermal habitats were more prevalent across allopatric than sympatric population pairs. These findings suggest that morphological divergence in response to thermal habitat, despite being relatively complex and multivariate, are predictable to a degree. Our data also suggest that the potential for migration of individuals between different thermal habitats may enhance nonparallel evolution and reduce our ability to predict responses to climate change.

A warmer environment can reduce sociability in an ectotherm.

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.

The role of vital dietary biomolecules in eco-evo-devo dynamics.

The physiological dependence of animals on dietary intake of vitamins, amino acids, and fatty acids is ubiquitous. Sharp differences in the availability of these vital dietary biomolecules among different resources mean that consumers must adopt a range of strategies to meet their physiological needs. We review the emerging work on omega-3 long-chain polyunsaturated fatty acids, focusing predominantly on predator-prey interactions, to illustrate that trade-off between capacities to consume resources rich in vital biomolecules and internal synthesis capacity drives differences in phenotype and fitness of consumers. This can then feedback to impact ecosystem functioning. We outline how focus on vital dietary biomolecules in eco-eco-devo dynamics can improve our understanding of anthropogenic changes across multiple levels of biological organization.

Fish vulnerability to capture by trapping is modulated by individual parasite density.

Commercial fishery harvest is a powerful evolutionary agent, but we know little about whether environmental stressors affect harvest-associated selection. We test how parasite infection relates to trapping vulnerability through selective processes underlying capture. We used fish naturally infected with parasites, including trematodes causing black spots under fish skin. We first assessed how individual parasite density related to standard metabolic rate (SMR), maximum metabolic rate (MMR) and absolute aerobic scope (AAS)-then used laboratory fishing simulations to test how capture vulnerability was related to parasite density. We further explored group-trapping dynamics using experimental shoals containing varying proportions of infected fish (groups of six with either 0, 2, 4 or 6 infected individuals). At the individual level, we found a positive relationship between parasite presence and SMR, but not MMR or AAS. While we saw no relationship between individual metabolic capacity and vulnerability to trapping, we found the length of time fish spent in traps increased with increasing parasite density, a predictor of trapping-related capture probability. At the group level, the number of infected individuals in a shoal did not affect overall group trapping vulnerability. Our results suggest that parasite infection has some capacity to shift individual vulnerability patterns in fisheries, and potentially influence the evolutionary outcomes of fisheries-induced evolution.

Aerobic scope in fishes with different lifestyles and across habitats: Trade-offs among hypoxia tolerance, swimming performance and digestion.

Exercise and aerobic scope in fishes have attracted scientists' attention for several decades. While it has been suggested that aerobic scope may limit behavioral expression and tolerance to environmental stressors in fishes, the exact importance of aerobic scope in an ecological context remains poorly understood. In this review, we examine the ecological relevance of aerobic scope by reconsidering and reanalyzing the existing literature on Chinese freshwater fishes across a wide-range of habitats and lifestyles. The available evidence suggests that natural selection in fast-flowing aquatic habitats may favor species with a high aerobic scope and anaerobic capacity for locomotion, whereas in relatively slow-flowing habitats, hypoxia tolerance may be favored at the cost of reduced locomotor capacity. In addition, while physical activity can usually cause fishes from fast-flowing habitats to reach their aerobic metabolic ceiling (i.e., maximum metabolic rate), possibly due to selection pressure on locomotion, most species from slow-flowing habitats can only reach their metabolic ceiling during digestion, either alone or in combination with physical activity. Overall, we suggest that fish exhibit a continuum of metabolic types, from a 'visceral metabolic type' with a higher digestive performance to a 'locomotion metabolic type' which appears to have reduced capacity for digestion but enhanced locomotor performance. Generally, locomotor-type species can either satisfy the demands of their high swimming capacity with a high oxygen uptake capacity or sacrifice digestion while swimming. In contrast, most visceral-type species show a pronounced decrease in swimming performance while digesting, probably owing to conflicts within their aerobic scope. In conclusion, the ecological relevance of aerobic scope and the consequent effects on other physiological functions are closely related to habitat and the lifestyle of a given species. These results suggest that swimming performance, digestion and hypoxia tolerance might coevolve due to dependence on metabolic traits such as aerobic scope.

Big-data approaches lead to an increased understanding of the ecology of animal movement.

Understanding animal movement is essential to elucidate how animals interact, survive, and thrive in a changing world. Recent technological advances in data collection and management have transformed our understanding of animal "movement ecology" (the integrated study of organismal movement), creating a big-data discipline that benefits from rapid, cost-effective generation of large amounts of data on movements of animals in the wild. These high-throughput wildlife tracking systems now allow more thorough investigation of variation among individuals and species across space and time, the nature of biological interactions, and behavioral responses to the environment. Movement ecology is rapidly expanding scientific frontiers through large interdisciplinary and collaborative frameworks, providing improved opportunities for conservation and insights into the movements of wild animals, and their causes and consequences.

Simulated trapping and trawling exert similar selection on fish morphology.

Commercial fishery harvest can influence the evolution of wild fish populations. Our knowledge of selection on morphology is however limited, with most previous studies focusing on body size, age, and maturation. Within species, variation in morphology can influence locomotor ability, possibly making some individuals more vulnerable to capture by fishing gears. Additionally, selection on morphology has the potential to influence other foraging, behavioral, and life-history related traits. Here we carried out simulated fishing using two types of gears: a trawl (an active gear) and a trap (a passive gear), to assess morphological trait-based selection in relation to capture vulnerability. Using geometric morphometrics, we assessed differences in shape between high and low vulnerability fish, showing that high vulnerability individuals display shallower body shapes regardless of gear type. For trawling, low vulnerability fish displayed morphological characteristics that may be associated with higher burst-swimming, including a larger caudal region and narrower head, similar to evolutionary responses seen in fish populations responding to natural predation. Taken together, these results suggest that divergent selection can lead to phenotypic differences in harvested fish populations.

The Potential for Physiological Performance Curves to Shape Environmental Effects on Social Behavior.

As individual animals are exposed to varying environmental conditions, phenotypic plasticity will occur in a vast array of physiological traits. For example, shifts in factors such as temperature and oxygen availability can affect the energy demand, cardiovascular system, and neuromuscular function of animals that in turn impact individual behavior. Here, we argue that nonlinear changes in the physiological traits and performance of animals across environmental gradients-known as physiological performance curves-may have wide-ranging effects on the behavior of individual social group members and the functioning of animal social groups as a whole. Previous work has demonstrated how variation between individuals can have profound implications for socially living animals, as well as how environmental conditions affect social behavior. However, the importance of variation between individuals in how they respond to changing environmental conditions has so far been largely overlooked in the context of animal social behavior. First, we consider the broad effects that individual variation in performance curves may have on the behavior of socially living animals, including: (1) changes in the rank order of performance capacity among group mates across environments; (2) environment-dependent changes in the amount of among- and within-individual variation, and (3) differences among group members in terms of the environmental optima, the critical environmental limits, and the peak capacity and breadth of performance. We then consider the ecological implications of these effects for a range of socially mediated phenomena, including within-group conflict, within- and among group assortment, collective movement, social foraging, predator-prey interactions and disease and parasite transfer. We end by outlining the type of empirical work required to test the implications for physiological performance curves in social behavior.

Genomic basis of fishing-associated selection varies with population density.

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.

Social Group Size and Shelter Availability Influence Individual Metabolic Traits in a Social Fish.

Group living is widespread among animal species and yields both costs and benefits. Presence of conspecifics can restrict or enhance the expression of individual behavior, and the recent social environment is thought to affect behavioral responses in later contexts, even when individuals are alone. However, little is known about how social group size influences the expression of individual physiological traits, including metabolic rates. There is some evidence that shoaling can reduce fish metabolic rates but this variable may be affected by habitat conditions such as shelter availability via density-dependent processes. We investigated how social group size and shelter availability influence Eurasian minnow (Phoxinus phoxinus) metabolic rates estimated by respirometry. Respirometry trials were conducted on fish in isolation before and after they were housed for 3 weeks in a social treatment consisting in a specific group size (n = 4 or 8) and shelter availability (presence or absence of plant shelter in the experimental tank). Plant shelter was placed over respirometers for half of the duration of the respirometry trials, allowing estimation of minimum daytime and nighttime metabolic rates in both conditions (in the presence or absence of plant shelter). Standard metabolic rate (SMR), maximum metabolic rate (MMR), and aerobic scope were also estimated over the entire trial. Minimum daytime and nighttime metabolic rates estimated while in presence of plant shelter were lower than when estimated in absence of plant shelter, both before and after individuals were housed in their social treatment. After the social treatment, SMRs were higher for fish that were held in groups of 4 as compared with those of fish held in groups of 8, while MMR showed no difference. Plant shelter availability during the social treatments did not influence SMR or MMR. Our results suggest that social group size may directly influence energy demands of individuals, highlighting the importance of understanding the role of group size on variations in physiological traits associated with energy expenditure.

Pour les animaux sociaux, la vie en groupe est associée à plusieurs coûts et bénéfices. La présence de congénères peut limiter ou amplifier l'expression des comportements individuels. L'environnement social peut également affecter les réponses comportementales ultérieures d'un individu dans d'autres contextes, même lorsqu'il se retrouve seul. Or, les effets de l'environnement social sur l'expression des traits physiologiques individuels, comme les taux métaboliques, sont très peu connus. La vie en banc pourrait réduire les taux métaboliques des poissons. Cela dit, la compétition pour des composantes limitantes de l'habitat comme la présence de refuges pourrait influencer les taux métaboliques individuels. L'objectif de cette étude était de quantifier et de comparer les effets de l'environnement social et de la présence de refuges sur les taux métaboliques des ménés communs Phoxinus phoxinus estimés par respirométrie. Notre design expérimental consistait en une expérience sociale de trois semaines précédée et suivie par des expériences de respirométrie. Durant l'expérience sociale, les poissons étaient gardés en groupes de quatre ou huit poissons dans des aquariums qui contenaient un refuge (plante aquatique) ou non. Durant la respirométrie, les poissons étaient placés en isolation dans des chambres qui étaient couvertes par des plantes aquatiques pour la moitié de la durée des expériences. Ainsi, les taux métaboliques minimum de jour et de nuit, en présence ou en absence de refuge ont été estimés à chaque expérience, en plus des taux métaboliques standard (SMR) et maximum (MMR). Les taux métaboliques minimum de jour et de nuit estimés en présence de refuge étaient moins élevés que ceux estimés en absence de refuge, et ce, autant avant et après l'expérience sociale. Après l'expérience sociale, les SMR étaient plus élevés pour les poissons qui avaient été gardés en groupes de quatre que pour les poissons gardés en groupes de huit, alors qu'aucune différence n'a été observée pour les MMR. La présence de refuge dans les aquariums durant l'expérience sociale n'a pas influencé les taux métaboliques. Nos résultats démontrent que la taille des groupes peut influencer les dépenses énergétiques des individus, ce qui souligne l'importance de comprendre le rôle des dynamiques sociales sur les variations dans les traits métaboliques.