Greater male variability in daily energy expenditure develops through puberty.

There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decreasing GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

Variability in energy expenditure is much greater in males than females.

In mammals, trait variation is often reported to be greater among males than females. However, to date, mainly only morphological traits have been studied. Energy expenditure represents the metabolic costs of multiple physical, physiological, and behavioral traits. Energy expenditure could exhibit particularly high greater male variation through a cumulative effect if those traits mostly exhibit greater male variation, or a lack of greater male variation if many of them do not. Sex differences in energy expenditure variation have been little explored. We analyzed a large database on energy expenditure in adult humans (1494 males and 3108 females) to investigate whether humans have evolved sex differences in the degree of interindividual variation in energy expenditure. We found that, even when statistically comparing males and females of the same age, height, and body composition, there is much more variation in total, activity, and basal energy expenditure among males. However, with aging, variation in total energy expenditure decreases, and because this happens more rapidly in males, the magnitude of greater male variation, though still large, is attenuated in older age groups. Considerably greater male variation in both total and activity energy expenditure could be explained by greater male variation in levels of daily activity. The considerably greater male variation in basal energy expenditure is remarkable and may be explained, at least in part, by greater male variation in the size of energy-demanding organs. If energy expenditure is a trait that is of indirect interest to females when choosing a sexual partner, this would suggest that energy expenditure is under sexual selection. However, we present a novel energetics model demonstrating that it is also possible that females have been under stabilizing selection pressure for an intermediate basal energy expenditure to maximize energy available for reproduction.

Individual variation in heat substitution: is activity in the cold energetically cheaper for some individuals than others?

In many endotherms, a potentially important yet often overlooked mechanism to save energy is the use of the heat generated by active skeletal muscles to replace heat that would have been generated by thermogenesis (i.e. 'activity-thermoregulatory heat substitution'). While substitution has been documented numerous times, the extent of individual variation in substitution has never been quantified. Here, we used a home-cage respirometry system to repeatedly measure substitution through the concomitant monitoring of metabolic rate (MR) and locomotor activity in 46 female white-footed mice (Peromyscus leucopus). A total of 117 measures of substitution were taken by quantifying the difference in the slope of the relationship between MR and locomotor activity speed at two different ambient temperatures. Consistency repeatability (±s.e.) of substitution was 0.313 (±0.131); hence, about a third of the variation in substitution occurs at the among-individual level. Body length and heart mass were positively correlated with substitution whereas surface area was negatively correlated with substitution. These three sub-organismal traits accounted for the majority of the among-individual variation (i.e. individual differences in substitution were not significant after accounting for these traits). Overall, our results imply that the energetic cost of activity below the thermoneutral zone is consistently cheaper from some individuals than others, and that the energy saved from substitution might be available to invest in fitness-enhancing activities.

A quantitative genetics perspective on the body-mass scaling of metabolic rate.

Widely observed allometric scaling (log-log slope<1) of metabolic rate (MR) with body mass (BM) in animals has been frequently explained using functional mechanisms, but rarely studied from the perspective of multivariate quantitative genetics. This is unfortunate, given that the additive genetic slope (bA) of the MR-BM relationship represents the orientation of the 'line of least genetic resistance' along which MR and BM may most likely evolve. Here, we calculated bA in eight species. Although most bA values were within the range of metabolic scaling exponents reported in the literature, uncertainty of each bA estimate was large (only one bA was significantly lower than 3/4 and none were significantly different from 2/3). Overall, the weighted average for bA (0.667±0.098 95% CI) is consistent with the frequent observation that metabolic scaling exponents are negatively allometric in animals (b<1). Although bA was significantly positively correlated with the phenotypic scaling exponent (bP) across the sampled species, bP was usually lower than bA, as reflected in a (non-significantly) lower weighted average for bP (0.596±0.100). This apparent discrepancy between bA and bP resulted from relatively shallow MR-BM scaling of the residuals [weighted average residual scaling exponent (be)=0.503±0.128], suggesting regression dilution (owing to measurement error and within-individual variance) causing a downward bias in bP. Our study shows how the quantification of the genetic scaling exponent informs us about potential constraints on the correlated evolution of MR and BM, and by doing so has the potential to bridge the gap between micro- and macro-evolutionary studies of scaling allometry.

Sex-specific genetic (co)variances of standard metabolic rate, body mass and locomotor activity in Drosophila melanogaster.

A longstanding focus in evolutionary physiology concerns the causes and consequences of variation in maintenance metabolism. Insight into this can be gained by estimating the sex-specific genetic architecture of maintenance metabolism alongside other, potentially correlated traits on which selection may also act, such as body mass and locomotor activity. This may reveal potential genetic constraints affecting the evolution of maintenance metabolism. Here, we used a half-sibling breeding design to quantify the sex-specific patterns of genetic (co)variance in standard metabolic rate (SMR), body mass and daily locomotor activity in Drosophila melanogaster. There was detectable additive genetic variance for all traits in both sexes. As expected, SMR and body mass were strongly and positively correlated, with genetic allometry exponents (bA  ± SE) that were close to 2/3 in females (0.66 ± 0.16) and males (0.58 ± 0.32). There was a significant and positive genetic correlation between SMR and locomotor activity in males, suggesting that alleles that increase locomotion have pleiotropic effects on SMR. Sexual differences in the genetic architecture were largely driven by a difference in genetic variance in locomotor activity between the sexes. Overall, genetic variation was mostly shared between males and females, setting the stage for a potential intralocus sexual conflict in the face of sexually antagonistic selection.

Metabolic rates of aggressive and submissive phenotypes are colour blind in the polymorphic Gouldian finch.

Evidence from a number of species suggests that behaviours associated with social rank are positively correlated with metabolic rate. These studies, however, are based on metabolic measurements of isolated individuals, thereby ignoring potential effects of social interactions on metabolic rates. Here, we characterised three pertinent metabolic indices in the two predominant genetic colour morphs of the Gouldian finch (Erythrura gouldiae): diurnal resting metabolic rate (RMR), nocturnal basal metabolic rate (BMR) and exercise-induced maximal metabolic rate (MMR). Research reveals that red-headed morphs consistently dominate the less aggressive black-headed morphs and that the two morphs differ in other behavioural and physiological traits. We measured daytime RMR of intermorph naïve birds (first-year virgin males maintained in total isolation from opposite colour morphs) and their metabolic responses to viewing a socially unfamiliar bird of each colour. Subsequently, each bird was placed in a home cage with an opposite colour morph (intermorph exposed) and the series of measurements was repeated. Daytime RMR was indistinguishable between the two morphs, regardless of whether they were intermorph naïve or intermorph exposed. However, both red- and black-headed birds showed a greater short-term increase in metabolic rate when viewing an unfamiliar red-headed bird than when seeing a black-headed bird, but only when intermorph naïve. Measurements of BMR and exercise-induced MMR did not differ between the two morphs, and consequently, aerobic scope was indistinguishable between them. We propose that the behavioural differences between these two sympatric morphs are functionally complementary and represent evolutionary stable strategies permitting establishment of dominance status in the absence of metabolic costs.

Phylogenetic analysis of macroecological patterns of home range area in snakes.

A home range is the area animals use to carry out routine activities such as mating, foraging, and caring for young. Thus, the area of a home range is an important indicator of an animal's behavioural and energetic requirements. While several studies have identified the factors that influence home range area (HRA), none of them has investigated global patterns of HRA among and within snake species. Here, we used a phylogenetic mixed model to determine which factors influence HRA in 51 snake species. We analysed 200 HRA estimates to test the influence of body mass, sex, age, diet, precipitation, latitude, winter and summer temperature, while controlling for the duration of the study and sample size. We found that males had larger HRA than females, that adults had larger HRA than juveniles, and that snake species with fish-based diets had smaller HRA than snake species with terrestrial vertebrate-based and invertebrate-based diets. We also found that HRA tended to increase as mean winter temperature decreases and tended to decrease with precipitation. After accounting for these factors, the phylogenetic heritability of HRA in snakes was low (0.21 ± 0.14). Determining the factors that dictate macroecological patterns of space use has important management implications in an era of rapid climate change.

How general is cognitive ability in non-human animals? A meta-analytical and multi-level reanalysis approach.

General intelligence has been a topic of high interest for over a century. Traditionally, research on general intelligence was based on principal component analyses and other dimensionality reduction approaches. The advent of high-speed computing has provided alternative statistical tools that have been used to test predictions of human general intelligence. In comparison, research on general intelligence in non-human animals is in its infancy and still relies mostly on factor-analytical procedures. Here, we argue that dimensionality reduction, when incorrectly applied, can lead to spurious results and limit our understanding of ecological and evolutionary causes of variation in animal cognition. Using a meta-analytical approach, we show, based on 555 bivariate correlations, that the average correlation among cognitive abilities is low (r = 0.185; 95% CI: 0.087-0.287), suggesting relatively weak support for general intelligence in animals. We then use a case study with relatedness (genetic) data to demonstrate how analysing traits using mixed models, without dimensionality reduction, provides new insights into the structure of phenotypic variance among cognitive traits, and uncovers genetic associations that would be hidden otherwise. We hope this article will stimulate the use of alternative tools in the study of cognition and its evolution in animals.

Repeatability of behavior and physiology: No impact of reproductive investment.

Animals have well-documented individual differences in their behaviour, including in their response to stressful stimuli. The physiological bases for the repeatability of these traits has been the focus of much research in recent years, in an attempt to explain the mechanistic drivers for behavioral syndromes. Whilst a range of studies have demonstrated repeatable individual differences in physiological traits, little is known about potential trade-offs between reproductive investment and the physiological responses to subsequent stressors. We therefore sought to test the behavioral and physiological responses of male zebra finches (Taeniopygia guttata) to a novel environment, quantifying a series of repeated "temporal reaction norms" before and after reproduction. Given that reproductive investment is costly both in time and energy, it is likely to affect expression of behavioral and physiological traits. We hypothesised that reproductive investment would impact the consistency of these temporal reaction norms. Specifically, we predicted that individuals which invested more in reproduction would show altered rates of habituation to a stressful stimulus. Therefore, we quantified temporal reaction norm components (i.e., intercept and slope) of two behaviours and metabolic rate (MR) within and among individuals before and after a breeding season. We found that individuals consistently differed in how their locomotor and feeding activity increased upon introduction into a novel environment and also how their MR decreased after being handled and confined within the metabolic chamber. We also found that the slope of the feeding activity reaction norm was negatively correlated with stress-induced corticosterone levels at the within-individual level. Finally, in contrast to our prediction, we found that neither the intercept nor slope of the reaction norms were influenced by the reproductive effort (the number of fledglings produced) displayed by individual males. This suggests that the substantial individual variation in the expression of physiological and behavioural traits is not plastic with respect to the immediate consequences of reproductive investment. This study is the first quantification of metabolic rate reaction norms and their relationships with fitness, which represents an important first step towards understanding the evolutionary significance of instantaneous habituation to stressful and novel situations.

Sex-Specific Among-Individual Covariation in Locomotor Activity and Resting Metabolic Rate in Drosophila melanogaster.

A key endeavor in evolutionary physiology is to identify sources of among- and within-individual variation in resting metabolic rate (RMR). Although males and females often differ in whole-organism RMR due to sexual size dimorphism, sex differences in RMR sometimes persist after conditioning on body mass, suggesting phenotypic differences between males and females in energy-expensive activities contributing to RMR. One potential difference is locomotor activity, yet its relationship with RMR is unclear and different energy budget models predict different associations. We quantified locomotor activity (walking) over 24 h and RMR (overnight) in 232 male and 245 female Drosophila melanogaster that were either mated or maintained as virgins between two sets of measurements. Accounting for body mass, sex, and reproductive status, RMR and activity were significantly and moderately repeatable (RMR: R=0.33±0.06; activity: R=0.58±0.03). RMR and activity were positively correlated among (rind=0.26±0.09) but not within (re=0.05±0.06) individuals. Moreover, activity varied throughout the day and between the sexes. Partitioning our analysis by sex and activity by time of day revealed that all among-individual correlations were positive and significant in males but nonsignificant or even significantly negative in females. Such differences in the RMR-activity covariance suggest fundamental differences in how the sexes manage their energy budget.

I Smell a Mouse: Indirect Genetic Effects on Voluntary Wheel-Running Distance, Duration and Speed.

Indirect genetic effects (IGEs; the heritable influence of one organism on a conspecific) can affect the evolutionary dynamics of complex traits, including behavior. Voluntary wheel running is an important model system in quantitative genetic studies of behavior, but the possibility of IGEs on wheel running and its components (time spent running and average running speed) has not been examined. Here, we analyze a dataset from a replicated selection experiment on wheel running (11,420 control and 26,575 selected mice measured over 78 generations) in which the standard measurement protocol allowed for the possibility of IGEs occurring through odors because mice were provided with clean cages attached to a clean wheel or a wheel previously occupied by another mouse for 6 days. Overall, mice ran less on previously occupied wheels than on clean wheels, and they ran significantly less when following a male than a female. Significant interactions indicated that the reduction in running was more pronounced for females than males and for mice from selected lines than control mice. Pedigree-based "animal model" analyses revealed significant IGEs for running distance (the trait under selection), with effect sizes considerably higher for the initial/exploratory phase (i.e., first two of six test days). Our results demonstrate that IGEs can occur in mice interacting through scent only, possibly because they attempt to avoid conspecifics.

Hif-1α paralogs play a role in the hypoxic ventilatory response of larval and adult zebrafish (Danio rerio).

Hypoxia-inducible factor (Hif) 1α, an extensively studied transcription factor, is involved in the regulation of many biological processes in hypoxia including the hypoxic ventilatory response. In zebrafish, there are two paralogs of Hif-1α (Hif-1A and Hif-1B), but little is known about the specific roles or potential sub-functionalization of the paralogs in response to hypoxia. Using knockout lines of Hif-1α paralogs, we examined their involvement in the hypoxic ventilatory response, measured as ventilation frequency (fV) in larval and adult zebrafish (Danio rerio). In wild-type zebrafish, fV increased across developmental time (4, 7, 10 and 15 days post--fertilization, dpf) in response to hypoxia (55 mmHg). In contrast, the Hif-1B knockout fish did not exhibit an increase in hypoxic fV at 4 dpf. Similar to wild-type, as larvae of all knockout lines developed, the magnitude of fV increased but to a lesser degree than in the wild-type larvae, until 15 dpf at which point there was no difference among the genotypes. In adult zebrafish, only in Hif-1B knockout fish was there an attenuation in fV during sustained exposure to 30 mmHg for 1 h but there was no effect when fish were exposed for a shorter duration to progressive hypoxia. The mechanism of action of Hif-1α, in part, may be through its downstream target, nitric oxide synthase, and its product, nitric oxide. Overall, the effect of each Hif-1α paralog on the hypoxic ventilatory response of zebrafish varies over development and is dependent on the type of hypoxic stress.

Performance trade-offs in wild mice.

Various aspects of performance (e.g., speed, strength, endurance) are thought to be important determinants of the success of animals in natural activities such as foraging, mating, and escaping from predators. However, it is generally known that morphological properties enhancing one type of performance (e.g., strength) can lead to a reduction in another (e.g., speed). Such performance trade-offs have been quantified at the inter-specific level, but evidence at the individual level remains equivocal. To test for the presence of a performance trade-off, we repeatedly captured a total of 189 wild white-footed mice (Peromyscus leucopus) and measured their grip strength and sprint speed. Using the maximum performance score obtained for each individual across all their repeated tests, we obtained a counter-intuitive (and biased) positive and highly significant phenotypic correlation. Using a bivariate mixed model, we detected a significant negative among-individual correlation between grip strength and sprint speed. By contrast, the within-individual correlation was positive but non-significant, thus illustrating the importance of properly partitioning the correlations at the among- and within-individual levels when testing for the presence of a performance trade-off. This study is one of the first to detect a performance trade-off at the among-individual level in a wild animal population. Such a trade-off may be caused by individual differences in muscle physiology and scapular morphology resulting from genetic differences and/or plastic responses to differential use of the arboreal vs. terrestrial parts of the environment.

Performance trade-offs and ageing in the 'world's greatest athletes'.

The mechanistic foundations of performance trade-offs are clear: because body size and shape constrains movement, and muscles vary in strength and fibre type, certain physical traits should act in opposition with others (e.g. sprint versus endurance). Yet performance trade-offs are rarely detected, and traits are often positively correlated. A potential resolution to this conundrum is that within-individual performance trade-offs can be masked by among-individual variation in 'quality'. Although there is a current debate on how to unambiguously define and account for quality, no previous studies have partitioned trait correlations at the within- and among-individual levels. Here, we evaluate performance trade-offs among and within 1369 elite athletes that performed in a total of 6418 combined-events competitions (decathlon and heptathlon). Controlling for age, experience and wind conditions, we detected strong trade-offs between groups of functionally similar events (throwing versus jumping versus running) occurring at the among-individual level. We further modelled individual (co)variation in age-related plasticity of performance and found previously unseen trade-offs in throwing versus running performance that manifest through ageing. Our results verify that human performance is limited by fundamental genetic, environmental and ageing constraints that preclude the simultaneous improvement of performance in multiple dimensions. Identifying these constraints is fundamental to understanding performance trade-offs and predicting the ageing of motor function.

Multiscale Evaluation of Thermal Dependence in the Glucocorticoid Response of Vertebrates.

Environmental temperature has profound effects on animal physiology, ecology, and evolution. Glucocorticoid (GC) hormones, through effects on phenotypic performance and life history, provide fundamental vertebrate physiological adaptations to environmental variation, yet we lack a comprehensive understanding of how temperature influences GC regulation in vertebrates. Using field studies and meta- and comparative phylogenetic analyses, we investigated how acute change and broadscale variation in temperature correlated with baseline and stress-induced GC levels. Glucocorticoid levels were found to be temperature and taxon dependent, but generally, vertebrates exhibited strong positive correlations with acute changes in temperature. Furthermore, reptile baseline, bird baseline, and capture stress-induced GC levels to some extent covaried with broadscale environmental temperature. Thus, vertebrate GC function appears clearly thermally influenced. However, we caution that lack of detailed knowledge of thermal plasticity, heritability, and the basis for strong phylogenetic signal in GC responses limits our current understanding of the role of GC hormones in species' responses to current and future climate variation.

Demystifying animal 'personality' (or not): why individual variation matters to experimental biologists.

Animal 'personality', defined as repeatable inter-individual differences in behaviour, is a concept in biology that faces intense controversy. Critics argue that the field is riddled with terminological and methodological inconsistencies and lacks a sound theoretical framework. Nevertheless, experimental biologists are increasingly studying individual differences in physiology and relating these to differences in behaviour, which can lead to fascinating insights. We encourage this trend, and in this Commentary we highlight some of the benefits of estimating variation in (and covariation among) phenotypic traits at the inter- and intra-individual levels. We focus on behaviour while drawing parallels with physiological and performance-related traits. First, we outline some of the confusion surrounding the terminology used to describe repeatable inter-individual differences in behaviour. Second, we argue that acknowledging individual behavioural differences can help researchers avoid sampling and experimental bias, increase explanatory power and, ultimately, understand how selection acts on physiological traits. Third, we summarize the latest methods to collect, analyse and present data on individual trait variation. We note that, while measuring the repeatability of phenotypic traits is informative in its own right, it is only the first step towards understanding how natural selection and genetic architecture shape intra-specific variation in complex, labile traits. Thus, understanding how and why behavioural traits evolve requires linking repeatable inter-individual behavioural differences with core aspects of physiology (e.g. neurophysiology, endocrinology, energy metabolism) and evolutionary biology (e.g. selection gradients, heritability).

Evolution of the additive genetic variance-covariance matrix under continuous directional selection on a complex behavioural phenotype.

Given the pace at which human-induced environmental changes occur, a pressing challenge is to determine the speed with which selection can drive evolutionary change. A key determinant of adaptive response to multivariate phenotypic selection is the additive genetic variance-covariance matrix ( G: ). Yet knowledge of G: in a population experiencing new or altered selection is not sufficient to predict selection response because G: itself evolves in ways that are poorly understood. We experimentally evaluated changes in G: when closely related behavioural traits experience continuous directional selection. We applied the genetic covariance tensor approach to a large dataset (n = 17 328 individuals) from a replicated, 31-generation artificial selection experiment that bred mice for voluntary wheel running on days 5 and 6 of a 6-day test. Selection on this subset of G: induced proportional changes across the matrix for all 6 days of running behaviour within the first four generations. The changes in G: induced by selection resulted in a fourfold slower-than-predicted rate of response to selection. Thus, selection exacerbated constraints within G: and limited future adaptive response, a phenomenon that could have profound consequences for populations facing rapid environmental change.

Tough decisions: Reproductive timing and output vary with individuals' physiology, behavior and past success in a social opportunistic breeder.

This article is part of a Special Issue "SBN 2014". Photoperiod and the hormonal response it triggers are key determinants of reproductive timing in birds. However, other cues and physiological traits may permit flexibility in the timing of breeding and perhaps facilitate adaptation to global change. Opportunistic breeders are excellent models to study the adaptive significance of this flexibility, especially at the individual level. Here, we sought to quantify whether particular male physiological and behavioral traits were linked to reproductive timing and output in wild-derived zebra finches. We repeatedly assessed male stress-induced corticosterone levels (CORT), basal metabolic rate (BMR), and activity before releasing them into outdoor aviaries and quantifying each pair's breeding timing, investment, and output over a seven-month period. Despite unlimited access to food and water, the colony breeding activity occurred in waves, probably due to interpair social stimulations. Pairs adjusted their inter-clutch interval and clutch size to social and temperature cues, respectively, but only after successful breeding attempts, suggesting a facultative response to external cues. When these effects were controlled for statistically or experimentally, breeding intervals were repeatable within individuals across reproductive attempts. In addition, males' first laying date and total offspring production varied with complex interactions between pre-breeding CORT, BMR and activity levels. These results suggest that no one trait is under selection but that, instead, correlational selection acts on hormone levels, metabolism, and behavior. Together our results suggest that studying inter-individual variation in breeding strategy and their multiple physiological and behavioral underpinnings may greatly improve our understanding of the mechanisms underlying the evolution of breeding decisions.

Among- and within-individual correlations between basal and maximal metabolic rates in birds.

The aerobic capacity model proposes that endothermy is a by-product of selection favouring high maximal metabolic rates (MMR) and its mechanistic coupling with basal metabolic rate (BMR). Attempts to validate this model in birds are equivocal and restricted to phenotypic correlations (rP), thus failing to distinguish among- and within-individual correlations (rind and re). We examined 300 paired measurements of BMR and MMR from 60 house sparrows before and after two levels of experimental manipulation - testosterone implants and immune challenge. Overall, repeatability was significant in both BMR (R=0.25±0.06) and MMR (R=0.52±0.06). Only the testosterone treatment altered the rP between BMR and MMR, which resulted from contrasting effects on rind and re. While rind was high and significant (0.62±0.22) in sham-implanted birds, re was negative and marginally non-significant (-0.15±0.09) in testosterone-treated birds. Thus, the expected mechanistic link between BMR and MMR was apparent, but only in birds with low testosterone levels.

Developmental stress can uncouple relationships between physiology and behaviour.

Phenotypic correlations (rP) have frequently been observed between physiological and behavioural traits, and the nature of these associations has been shown to be modulated by a range of environmental stressors. Studies to date have examined the effects of acute stressors on physiology-behaviour interrelations, but the potential for permanent changes induced by exposure to stress during development remains unexplored. We exposed female zebra finches to dietary restriction during the nestling stage and tested how this affected rP among a variety of physiological traits (haematocrit, stress-induced corticosterone level and basal metabolic rate (BMR)) and behavioural traits (activity and feeding rates in novel and familiar environments). Developmental stress completely uncoupled the relationship between activity in a novel environment and two physiological traits: haematocrit and BMR. This suggests that nutritionally based developmental stress has provoked changes in the energy budget that alleviate the trade-off between maintenance (BMR) and locomotor activities.