What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the ‘maintenance costs’ of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.     

Life-History and Spatial Determinants of Somatic Growth Dynamics in Komodo Dragon Populations

Somatic growth patterns represent a major component of organismal fitness and may vary among sexes and populations due to genetic and environmental processes leading to profound differences in life-history and demography. This study considered the ontogenic, sex-specific and spatial dynamics of somatic growth patterns in ten populations of the world’s largest lizard the Komodo dragon (Varanus komodoensis). The growth of 400 individual Komodo dragons was measured in a capture-mark-recapture study at ten sites on four islands in eastern Indonesia, from 2002 to 2010. Generalized Additive Mixed Models (GAMMs) and information-theoretic methods were used to examine how growth rates varied with size, age and sex, and across and within islands in relation to site-specific prey availability, lizard population density and inbreeding coefficients. Growth trajectories differed significantly with size and between sexes, indicating different energy allocation tactics and overall costs associated with reproduction. This leads to disparities in maximum body sizes and longevity. Spatial variation in growth was strongly supported by a curvilinear density-dependent growth model with highest growth rates occurring at intermediate population densities. Sex-specific trade-offs in growth underpin key differences in Komodo dragon life-history including evidence for high costs of reproduction in females. Further, inverse density-dependent growth may have profound effects on individual and population level processes that influence the demography of this species.     

Starvation reveals the cause of infection-induced castration and gigantism

Parasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna–Pasteuria ramosa host–parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.     

Carryover effects from environmental change in early life: An overlooked driver of the amphibian extinction crisis?

Ecological carryover effects, or delayed effects of the environment on an organism's phenotype, are central predictors of individual fitness and a key issue in conservation biology. Climate change imposes increasingly variable environmental conditions that may be challenging to early life-history stages in animals with complex life histories, leading to detrimental physiological and fitness effects in later life. Yet, the latent nature of carryover effects, combined with the long temporal scales over which they can manifest, means that this phenomenon remains understudied and is often overlooked in short-term studies limited to single life-history stages. Herein, we review evidence for the physiological carryover effects induced by elevated ultraviolet radiation (UVR; 280–400 nm) as a potential contributor to recent amphibian population declines. UVR exposure causes a suite of molecular, cellular and physiological consequences known to underpin carryover effects in other taxa, but there is a lack of research linking embryonic and larval UVR exposures to fitness consequences post-metamorphosis in amphibians. We propose that the key impacts of UVR on disease-related amphibian declines are facilitated through carryover effects that bridge embryonic and larval UVR exposure with potential increased disease susceptibility post-metamorphosis. We conclude by identifying a practical direction for the study of ecological carryover effects in amphibians that could guide future ecological research in the broader field of conservation physiology. Only by addressing carryover effects can many of the mechanistic links between environmental change and population declines be elucidated.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

Life-history evolution and the origin of multicellularity

The fitness of an evolutionary individual can be understood in terms of its two basic components: survival and reproduction. As embodied in current theory, trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. Here, we argue that the evolution of germ-soma specialization and the emergence of individuality at a new higher level during the transition from unicellular to multicellular organisms are also consequences of trade-offs between the two components of fitness-survival and reproduction. The models presented here explore fitness trade-offs at both the cell and group levels during the unicellular-multicellular transition. When the two components of fitness negatively covary at the lower level there is an enhanced fitness at the group level equal to the covariance of components at the lower level. We show that the group fitness trade-offs are initially determined by the cell level trade-offs. However, as the transition proceeds to multicellularity, the group level trade-offs depart from the cell level ones, because certain fitness advantages of cell specialization may be realized only by the group. The curvature of the trade-off between fitness components is a basic issue in life-history theory and we predict that this curvature is concave in single-celled organisms but becomes increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the initial cost of reproduction to survival which increases as group size increases. To illustrate the principles and conclusions of the model, we consider aspects of the biology of the volvocine green algae, which contain both unicellular and multicellular members.     

Perceived social isolation,evolutionary fitness and health outcomes: a lifespan approach

Sociality permeates each of the fundamental motives of human existence and plays a critical role in evolutionary fitness across the lifespan. Evidence for this thesis draws from research linking deficits in social relationship—as indexed by perceived social isolation (i.e. loneliness)—with adverse health and fitness consequences at each developmental stage of life. Outcomes include depression, poor sleep quality, impaired executive function, accelerated cognitive decline, unfavourable cardiovascular function, impaired immunity, altered hypothalamic pituitary–adrenocortical activity, a pro-inflammatory gene expression profile and earlier mortality. Gaps in this research are summarized with suggestions for future research. In addition, we argue that a better understanding of naturally occurring variation in loneliness, and its physiological and psychological underpinnings, in non-human species may be a valuable direction to better understand the persistence of a ‘lonely’ phenotype in social species, and its consequences for health and fitness.     

Longevity and ageing: appraising the evolutionary consequences of growing old

Senescence or ageing is an increase in mortality and/or decline in fertility with increasing age. Evolutionary theories predict that ageing or longevity evolves in response to patterns of extrinsic mortality or intrinsic damage. If ageing is viewed as the outcome of the processes of behaviour, growth and reproduction then it should be possible to predict mortality rate. Recent developments have shown that it is now possible to integrate these ecological and physiological processes and predict the shape of mortality trajectories. By drawing on the key exciting developments in the cellular, physiological and ecological process of longevity the evolutionary consequences of ageing are reviewed. In presenting these ideas an evolutionary demographic framework is used to argue how trade-offs in life-history strategies are important in the maintenance of variation in longevity within and between species. Evolutionary processes associated with longevity have an important role in explaining levels of biological diversity and speciation. In particular, the effects of life-history trait trade-offs in maintaining and promoting species diversity are explored. Such trade-offs can alleviate the effects of intense competition between species and promote species coexistence and diversification. These results have important implications for understanding a number of core ecological processes such as how species are divided among niches, how closely related species co-occur and the rules by which species assemble into food-webs. Theoretical work reveals that the proximate physiological processes are as important as the ecological factors in explaining the variation in the evolution of longevity. Possible future research challenges integrating work on the evolution and mechanisms of growing old are briefly discussed.     

Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis

Variation in fitness generated by differences in functional performance can often be traced to morphological variation among individuals within natural populations. However, morphological variation itself is strongly influenced by environmental factors (e.g., temperature) and maternal effects (e.g., variation in egg size). Understanding the full ecological context of individual variation and natural selection therefore requires an integrated view of how the interaction between the environment and development structures differences in morphology, performance, and fitness. Here we use naturally occurring environmental and maternal variation in the frog Bombina orientalis in South Korea to show that ovum size, average temperature, and variance in temperature during the early developmental period affect body sizes, shapes, locomotor performance, and ultimately the probability of an individual surviving interspecific predation in predictable but nonadditive ways. Specifically, environmental variability can significantly change the relationship between maternal investment in offspring and offspring fitness so that increased maternal investment can actually negatively affect offspring over a broad range of environments. Integrating environmental variation and developmental processes into traditional approaches of studying phenotypic variation and natural selection is likely to provide a more complete picture of the ecological context of evolutionary change.     

Integrating animal behaviour into research on multiple environmental stressors: a conceptual framework

While a large body of research has focused on the physiological effects of multiple environmental stressors, how behavioural and life-history plasticity mediate multiple-stressor effects remains underexplored. Behavioural plasticity can not only drive organism-level responses to stressors directly but can also mediate physiological responses. Here, we provide a conceptual framework incorporating four fundamental trade-offs that explicitly link animal behaviour to life-history-based pathways for energy allocation, shaping the impact of multiple stressors on fitness. We first address how small-scale behavioural changes can either mediate or drive conflicts between the effects of multiple stressors and alternative physiological responses. We then discuss how animal behaviour gives rise to three additional understudied and interrelated trade-offs: balancing the benefits and risks of obtaining the energy needed to cope with stressors, allocation of energy between life-history traits and stressor responses, and larger-scale escape from stressors in space or time via large-scale movement or dormancy. Finally, we outline how these trade-offs interactively affect fitness and qualitative ecological outcomes resulting from multiple stressors. Our framework suggests that explicitly considering animal behaviour should enrich our mechanistic understanding of stressor effects, help explain extensive context dependence observed in these effects, and highlight promising avenues for future empirical and theoretical research.     

The biology hidden inside residual within‐individual phenotypic variation

Phenotypes vary hierarchically among taxa and populations, among genotypes within populations, among individuals within genotypes, and also within individuals for repeatedly expressed, labile phenotypic traits. This hierarchy produces some fundamental challenges to clearly defining biological phenomena and constructing a consistent explanatory framework. We use a heuristic statistical model to explore two consequences of this hierarchy. First, although the variation existing among individuals within populations has long been of interest to evolutionary biologists, within‐individual variation has been much less emphasized. Within‐individual variance occurs when labile phenotypes (behaviour, physiology, and sometimes morphology) exhibit phenotypic plasticity or deviate from a norm‐of‐reaction within the same individual. A statistical partitioning of phenotypic variance leads us to explore an array of ideas about residual within‐individual variation. We use this approach to draw attention to additional processes that may influence within‐individual phenotypic variance, including interactions among environmental factors, ecological effects on the fitness consequences of plasticity, and various types of adaptive variance. Second, our framework for investigating variation in phenotypic variance reveals that interactions between levels of the hierarchy form the preconditions for the evolution of all types of plasticity, and we extend this idea to the residual level within individuals, where both adaptive plasticity in residuals and canalization‐like processes (stability) can evolve. With the statistical tools now available to examine heterogeneous residual variance, an array of novel questions linking phenotype to environment can be usefully addressed.     

On the transfer of fitness from the cell to the multicellular organism

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ–soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae – which contain both unicellular and multicellular members – to illustrate the principles and conclusions discussed.     

Individual variation in baseline and stress-induced corticosterone and prolactin levels predicts parental effort by nesting mourning doves

Endocrine systems have an important mechanistic role in structuring life-history trade-offs. During breeding, individual variation in prolactin (PRL) and corticosterone (CORT) levels affects behavioral and physiological processes that drive trade-offs between reproduction and self-maintenance. We examined patterns in baseline (BL) and stress induced (SI; level following a standard capture-restraint protocol) levels of PRL and CORT for breeding mourning doves (Zenaida macroura). We determined whether the relationship of adult condition and parental effort to hormone levels in wild birds was consistent with life-history predictions. Both BL PRL and BL CORT level in adults were positively related to nestling weight at early nestling ages, consistent with the prediction of a positive relationship of hormone levels to current parental effort of adults and associated increased energy demand. Results are consistent with the two hormones acting together at baseline levels to limit negative effects of CORT on reproduction while maintaining beneficial effects such as increased foraging for nestling feeding. Our data did not support predictions that SI responses would vary in response to nestling or adult condition. The magnitude of CORT response in the parents to our capture-restraint protocol was negatively correlated with subsequent parental effort. Average nestling weights for adults with the highest SI CORT response were on average 10–15% lighter than expected for their age in follow-up visits after the stress event. Our results demonstrated a relationship between individual hormone levels and within population variation in parental effort and suggested that hormonal control plays an important role in structuring reproductive decisions for mourning doves.     

Can natural selection maintain long-distance dispersal? Insight from a stream salamander system

Dispersal distributions are often characterized by many individuals that stay close to their origin and large variation in the distances moved by those that leave. This variation in dispersal distance can strongly influence demographic, ecological, and evolutionary processes. However, a lack of data on the fitness and phenotype of individual dispersers has impeded research on the role of natural selection in maintaining variation in dispersal distance. Six years of spatially explicit capture-mark-recapture data showed that survival increased with dispersal distance in the stream salamander Gyrinophilus porphyriticus. To understand the evolutionary implications of this fitness response, we tested whether variation in dispersal distance has a phenotypic basis. We used photographs of marked individuals to measure head, trunk, and leg morphology. We then tested whether dispersal distances over the six-year study period were predicted by these traits. Dispersal distance was significantly related to leg morphology: individuals with relatively long forelimbs and short hindlimbs dispersed the farthest. These results support the hypothesis that positive fitness consequences maintain phenotypes enabling long-distance dispersal. More broadly, they suggest that natural selection can promote variation in dispersal distance and associated phenotypes, offering an alternative to the view that dispersal distance is driven by stochastic or landscape-specific mechanisms.     

Population divergence along lines of genetic variance and covariance in the invasive plant Lythrum salicaria in eastern North America

Evolution during biological invasion may occur over contemporary timescales, but the rate of evolutionary change may be inhibited by a lack of standing genetic variation for ecologically relevant traits and by fitness trade-offs among them. The extent to which these genetic constraints limit the evolution of local adaptation during biological invasion has rarely been examined. To investigate genetic constraints on life-history traits, we measured standing genetic variance and covariance in 20 populations of the invasive plant purple loosestrife (Lythrum salicaria) sampled along a latitudinal climatic gradient in eastern North America and grown under uniform conditions in a glasshouse. Genetic variances within and among populations were significant for all traits; however, strong intercorrelations among measurements of seedling growth rate, time to reproductive maturity and adult size suggested that fitness trade-offs have constrained population divergence. Evidence to support this hypothesis was obtained from the genetic variance-covariance matrix (G) and the matrix of (co)variance among population means (D), which were 79.8% (95% C.I. 77.7-82.9%) similar. These results suggest that population divergence during invasive spread of L. salicaria in eastern North America has been constrained by strong genetic correlations among life-history traits, despite large amounts of standing genetic variation for individual traits.     

Selective consequences of catastrophes for growth rates in a stream-dwelling salmonid

Optimal life histories in a fluctuating environment are likely to differ from those that are optimal in a constant environment, but we have little understanding of the consequences of bounded fluctuations versus episodic massive mortality events. Catastrophic disturbances, such as floods, droughts, landslides and fires, substantially alter the population dynamics of affected populations, but little has been done to investigate how catastrophes may act as a selective agent for life-history traits. We use an individual-based model of population dynamics of the stream-dwelling salmonid marble trout (Salmo marmoratus) to investigate how trade-offs between the growth and mortality of individuals and density-dependent body growth can lead to the maintenance of a wide or narrow range of individual variation in body growth rates in environments that are constant (i.e., only demographic stochasticity), variable (i.e., environmental stochasticity), or variable with catastrophic events that cause massive mortalities (e.g., flash floods). We find that occasional episodes of massive mortality can substantially reduce persistent variability in individual growth rates. Lowering the population density reduces density dependence and allows for higher fitness of more opportunistic strategies (rapid growth and early maturation) during the recovery period.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild

Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy–bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether ‘exploration behaviour’, a captive assay of the shy–bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.     

Positive genetic correlations among major life-history traits related to ecological success in the aphid Myzus persicae

Life-history theory is based on the assumption that evolution is constrained by trade-offs among different traits that contribute to fitness. Such trade-offs should be evident from negative genetic correlations among major life-history traits. However, this expectation is not always met. Here I report the results of a life-table experiment designed to measure the broad-sense heritabilities of life-history traits and their genetic correlations in 19 different clones of the aphid Myzus persicae from Victoria, Australia. Most individual traits, as well as fitness calculated as the finite rate of increase from the life table, exhibited highly significant heritabilities. The pattern of genetic correlations revealed absolutely no evidence for life-history trade-offs. Rather, life histories were arranged along an axis from better to worse. Clones with shorter development times tended to have larger body sizes, higher fecundities, and larger offspring. The fitness of clones estimated from the life table in the laboratory tended to be positively associated with their abundance in the field. Fitness also increased significantly with heterozygosity at the seven microsatellite loci that were used to distinguish clones and estimate their frequencies in the field. I discuss these findings in light of a recent proposition that positive genetic correlations among life-history traits for which trade-offs are expected can be explained by genetic variation for resource acquisition ability that is maintained in populations by a cost of acquisition, and I propose ways to test for such a cost in M. persicae.     

Fitness consequences of the timing of metamorphosis in a freshwater crustacean

Metamorphosis is a common life-cycle transition in organisms as diverse as amphibians, insects, fishes and crustaceans, and the timing of this transition often affects an individual's fitness. Here, we measured age and size at metamorphosis in laboratory-reared individuals of the freshwater copepod, Diaptomus leptopus , and then followed individuals over their entire life cycle to assess the fitness consequences of variation in age and size at metamorphosis. In 3 separate experiments, individuals were raised in different food conditions: low food (0.2 μg C/ml) switched to high food (0.7 μg C/ml), or high food switched to low food, at several different larval and juvenile stages. Control individuals were reared on high or low food concentrations over their entire life cycles. For each individual, we measured age and size at metamorphosis and age and size at maturity; for females, we also measured total lifetime egg production, longevity, and calculated a composite fitness measure, λ. Statistical analyses showed no significant effects of age or size at metamorphosis on these same traits measured at maturity, or on the fitness components we estimated. The first individuals to mature had the highest total egg production and individual fitness; differences in body size at maturation explained none of the variation observed in fitness components. Our results show that metamorphosis was uncoupled from maturity and from fitness components by growth and development achieved during the juvenile phase of the life cycle, and support the conclusion that fitness consequences of metamorphosis depend fundamentally on the organization of an organism's life cycle. They also suggest that body size plays a different life-history role in these organisms than is recognized in most poikilotherms, and suggest the hypothesis, based on laboratory experiments, that selection may act primarily on juvenile developmental rates in field populations.