Metabolic loads and the costs of metazoan reproduction.

Reproduction includes two energy investments-the energy in the offspring and the energy expended to make them. The former is well understood, whereas the latter is unquantified but often assumed to be small. Without understanding both investments, the true energy costs of reproduction are unknown. We present a framework for estimating the total energy costs of reproduction by combining data on the energy content of offspring (direct costs) and the metabolic load of bearing them (indirect costs). We find that direct costs typically represent the smaller fraction of the energy expended on reproduction. Mammals pay the highest reproductive costs (excluding lactation), ~90% of which are indirect. Ectotherms expend less on reproduction overall, and live-bearing ectotherms pay higher indirect costs compared with egg-layers. We show that the energy demands of reproduction exceed standard assumptions.

Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Per capita sperm metabolism is density dependent.

From bacteria to metazoans, higher density populations have lower per capita metabolic rates than lower density populations. The negative covariance between population density and metabolic rate is thought to represent a form of adaptive metabolic plasticity. A relationship between density and metabolism was actually first noted 100 years ago, and was focused on spermatozoa; even then, it was postulated that adaptive plasticity drove this pattern. Since then, contemporary studies of sperm metabolism specifically assume that sperm concentration has no effect on metabolism and that sperm metabolic rates show no adaptive plasticity. We did a systematic review to estimate the relationship between sperm aerobic metabolism and sperm concentration, for 198 estimates spanning 49 species, from protostomes to humans from 88 studies. We found strong evidence that per capita metabolic rates are concentration dependent: both within and among species, sperm have lower metabolisms in dense ejaculates, but increase their metabolism when diluted. On average, a 10-fold decrease in sperm concentration increased per capita metabolic rate by 35%. Metabolic plasticity in sperm appears to be an adaptive response, whereby sperm maximize their chances of encountering eggs.

Cold adaptation does not handicap warm tolerance in the most abundant Arctic seabird.

Arctic birds and mammals are physiologically adapted to survive in cold environments but live in the fastest warming region on the planet. They should therefore be most threatened by climate change. We fitted a phylogenetic model of upper critical temperature (TUC) in 255 bird species and determined that TUC for dovekies (Alle alle; 22.4°C)-the most abundant seabird in the Arctic-is 8.8°C lower than predicted for a bird of its body mass (150 g) and habitat latitude. We combined our comparative analysis with in situ physiological measurements on 36 dovekies from East Greenland and forward-projections of dovekie energy and water expenditure under different climate scenarios. Based on our analyses, we demonstrate that cold adaptation in this small Arctic seabird does not handicap acute tolerance to air temperatures up to at least 15°C above their current maximum. We predict that climate warming will reduce the energetic costs of thermoregulation for dovekies, but their capacity to cope with rising temperatures will be constrained by water intake and salt balance. Dovekies evolved 15 million years ago, and their thermoregulatory physiology might also reflect adaptation to a wide range of palaeoclimates, both substantially warmer and colder than the present day.

Temperature and nutrition do not interact to shape the evolution of metabolic rate.

Metabolic cold adaptation, or Krogh's rule, is the controversial hypothesis that predicts a monotonically negative relationship between metabolic rate and environmental temperature for ectotherms living along thermal clines measured at a common temperature. Macrophysiological patterns consistent with Krogh's rule are not always evident in nature, and experimentally evolved responses to temperature have failed to replicate such patterns. Hence, temperature may not be the sole driver of observed variation in metabolic rate. We tested the hypothesis that temperature, as a driver of energy demand, interacts with nutrition, a driver of energy supply, to shape the evolution of metabolic rate to produce a pattern resembling Krogh's rule. To do this, we evolved replicate lines of Drosophila melanogaster at 18, 25 or 28°C on control, low-calorie or low-protein diets. Contrary to our prediction, we observed no effect of nutrition, alone or interacting with temperature, on adult female and male metabolic rates. Moreover, support for Krogh's rule was only in females at lower temperatures. We, therefore, hypothesize that observed variation in metabolic rate along environmental clines arises from the metabolic consequences of environment-specific life-history optimization, rather than because of the direct effect of temperature on metabolic rate. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Thermoregulatory strategies of songbird nestlings reveal limited capacity for cooling and high risk of dehydration.

How the accelerating pace of global warming will affect animal populations depends on the effects of increasing temperature across the life cycle. Developing young are sensitive to environmental challenges, often with life-long consequences, but the risks of climate warming during this period are insufficiently understood. This may be due to limited insight into physiological sensitivity and the temperatures that represent a thermal challenge for young. Here we examined the physiological and behavioural effects of increasing temperatures by measuring metabolic rate, water loss, and heat dissipation behaviours between 25-45 °C in nestlings of a small free-living songbird of temperate SE-Australia, the superb fairy-wren. We found a high and relatively narrow thermoneutral zone from 33.1 to 42.3 °C, with metabolic rate increasing and all nestlings panting above this range. Evaporative water loss sharply increased above 33.5 °C; at the same temperature, nestlings changed their posture (extended their wings) to facilitate passive heat loss. However, at all temperatures measured, water loss was insufficient to dissipate metabolically produced heat, indicating poor cooling capabilities, which persisted even when individuals were panting. While nestlings are relatively tolerant to higher temperatures, with no evidence for hyperthermia at temperatures below 42 °C, they are at a high risk of dehydration even at lower temperatures, with limited ability to mitigate this. Thus, climate warming is likely to elevate the risk dehydration, which is concerning, since it is accompanied by drier conditions.

How and Why Does Metabolism Scale with Body Mass?

Most explanations for the relationship between body size and metabolism invoke physical constraints; such explanations are evolutionarily inert, limiting their predictive capacity. Contemporary approaches to metabolic rate and life history lack the pluralism of foundational work. Here, we call for reforging of the lost links between optimization approaches and physiology.

Linking physiology and climate to infer species distributions in Australian skinks.

Climate has a key impact on animal physiology, which in turn can have a profound influence on geographic distributions. Yet, the mechanisms linking climate, physiology and distribution are not fully resolved. Using an integrative framework, we tested the predictions of the climatic variability hypothesis (CVH), which states that species with broader distributions have broader physiological tolerance than range-restricted species, in a group of Lampropholis skinks (8 species, 196 individuals) along a latitudinal gradient in eastern Australia. We investigated several physiological aspects including metabolism, water balance, thermal physiology, thermoregulatory behaviour and ecological performance. Additionally, to test whether organismal information (e.g. behaviour and physiology) can enhance distribution models, hence providing evidence that physiology and climate interact to shape range sizes, we tested whether species distribution models incorporating physiology better predict the range sizes than models using solely climatic layers. In agreement with the CVH, our results confirm that widespread species can tolerate and perform better at broader temperature ranges than range-restricted species. We also found differences in field body temperatures, but not thermal preference, between widespread and range-restricted species. However, metabolism and water balance did not correlate with range size. Biophysical modelling revealed that the incorporation of physiological and behavioural data improves predictions of Lampropholis distributions compared with models based solely on macroclimatic inputs, but mainly for range-restricted species. By integrating several aspects of the physiology and niche modelling of a group of ectothermic animals, our study provides evidence that physiology correlates with species distributions. Physiological responses to climate are central in establishing geographic ranges of skinks, and the incorporation of processes occurring at local scales (e.g. behaviour) can improve species distribution models.

Long-term effects of incubation temperature on growth and thermal physiology in a small ectotherm.

Thermal conditions in the developmental environment can substantially affect an individual's phenotype, particularly in egg-laying ectotherms. However, whether these effects persist into adulthood is rarely examined. To investigate this, we incubated delicate skink, Lampropholis delicata, eggs at either cool (22°C), mild (26°C) or hot (30°C) temperatures. After hatching, we measured growth, thermal performance curves of locomotor activity, and thermal sensitivity of resting metabolic rate of offspring as juveniles (4-6 weeks of age), sub-adults (approx. 200 days of age), and adults (approx. 2 years of age), and then measured developmental temperature impacts on male fertility. Incubation temperature had a lasting effect on growth and locomotor performance, with cool and hot incubation temperatures resulting in faster growth and larger maximum size, and hot incubation temperatures reducing locomotor performance at all timepoints. Effects on resting metabolic rate were only present in sub-adults, with a higher metabolic rate at high and average body mass and negative metabolic scaling exponent in cool-incubated lizards. Additionally, cool and hot incubation treatments resulted in shorter sperm midpieces and heads. Incubation temperature did not affect testis mass or sperm count. Overall, our results demonstrate that incubation temperature can have lasting effects on later life stages, highlighting the importance of maternal nest-site selection, but that some effects are age dependent. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Does thermal biology differ between two colour pattern morphs of a widespread Australian lizard?

Alternative phenotypes allow individuals to pursue different adaptive pathways in response to the same selective challenge. Colour polymorphic species with geographically varying morph frequencies may reflect multiple adaptations to spatial variables such as temperature and climate. We examined whether thermal biology differed between colour morphs of an Australian lizard, the delicate skink, Lampropholis delicata. The delicate skink has two colour pattern morphs, with frequencies varying across latitude and sex: plain (darker, more common at temperate latitudes, more common in males) or striped (lighter, more common at lower latitudes, more common in females). We tested heating and cooling rate, sprint speed, thermal preference, field body temperature and metabolic rate in both morphs and sexes to determine any link between colour and morph frequency distribution. Plain individuals heated more quickly, but other thermal traits showed little variation among morphs. Lampropholis delicata colour influences rates of heat exchange, but the relationship does not appear to be adaptive, suggesting that behavioural thermoregulation homogenises body temperature in the field. While we find no substantial evidence of thermal differences between the two colour morphs, morph-specific behaviour may buffer against differences in heat exchange. Latitudinal variation in species colour may be driven by selection pressures other than temperature.

Life history optimisation drives latitudinal gradients and responses to global change in marine fishes.

Within many species, and particularly fish, fecundity does not scale with mass linearly; instead, it scales disproportionately. Disproportionate intraspecific size-reproduction relationships contradict most theories of biological growth and present challenges for the management of biological systems. Yet the drivers of reproductive scaling remain obscure and systematic predictors of how and why reproduction scaling varies are lacking. Here, we parameterise life history optimisation model to predict global patterns in the life histories of marine fishes. Our model predict latitudinal trends in life histories: Polar fish should reproduce at a later age and show steeper reproductive scaling than tropical fish. We tested and confirmed these predictions using a new, global dataset of marine fish life histories, demonstrating that the risks of mortality shape maturation and reproductive scaling. Our model also predicts that global warming will profoundly reshape fish life histories, favouring earlier reproduction, smaller body sizes, and lower mass-specific reproductive outputs, with worrying consequences for population persistence.

Optimisation and constraint: explaining metabolic patterns in biology.

Constraint-based explanations have dominated theories of size-related patterns in nature for centuries. Explanations for metabolic scaling - the way in which metabolism changes with body mass - have been based on the geometry of circulatory networks through which resources are distributed, the need to dissipate heat produced as a by-product of metabolic processes, and surface-area-to-volume constraints on the flux of nutrients or waste. As an alternative to these constraint-based approaches, we recently developed a new theory that predicts that metabolic allometry arises as a consequence of the optimisation of growth and reproduction to maximise fitness within a finite life. Our theory is free of physical geometric constraints that limit the possibilities available to evolution, and we therefore argue that metabolic allometry can be explained without the need to invoke any of the assumed constraints traditionally imposed by metabolic theories. Our findings also suggest that metabolism, growth and reproduction have co-evolved to maximise fitness (i.e. lifetime reproduction) and that the observed patterns in these fundamental characteristics of life can similarly be explained by optimisation rather than constraint. In this Centenary Commentary, we present an overview of our approach and a critique of its limitations. We propose a suite of empirical tests that we hope will move the field forward, discuss the dangers of model overparameterisation and highlight the need to remain open to non-adaptive hypotheses for the origin of biological patterns.

Response to Comments on "Metabolic scaling is the product of life-history optimization".

Froese and Pauly argue that our model is contradicted by the observation that fish reproduce before their growth rate decreases. Kearney and Jusup show that our model incompletely describes growth and reproduction for some species. Here we discuss the costs of reproduction, the relationship between reproduction and growth, and propose tests of models based on optimality and constraint.

Univariate and multivariate plasticity in response to incubation temperature in an Australian lizard.

Environments, particularly developmental environments, can generate a considerable amount of phenotypic variation through phenotypic plasticity. Plasticity in response to incubation temperature is well characterised in egg-laying reptiles. However, traits do not always vary independently of one another, and studies encompassing a broad range of traits spanning multiple categories are relatively rare but crucial to better understand whole-organism responses to environmental change, particularly if covariation among traits may constrain plasticity. In this study, we investigated multivariate plasticity in response to incubation across three temperatures in the delicate skink, Lampropholis delicata, and whether this was affected by covariation among traits. At approximately 1 month of age, a suite of growth, locomotor performance, thermal physiology and behavioural traits were measured. Plasticity in the multivariate phenotype of delicate skinks was distinct for different incubation temperatures. Cool temperatures drove shifts in growth, locomotor performance and thermal physiology, while hot temperatures primarily caused changes in locomotor performance and behaviour. These differences are likely due to variation in thermal reaction norms, as there was little evidence that covariation among traits or phenotypic integration influenced plasticity, and there was no effect of incubation temperature on the direction or strength of covariation. While there were broad themes in terms of which trait categories were affected by different incubation treatments, traits appeared to be affected independently by developmental temperature. Comparing reaction norms of a greater range of traits and temperatures will enable better insight into these patterns among trait categories, as well as the impacts of environmental change.

Macroevolutionary patterns in marine hermaphroditism.

Most plants and many animals are hermaphroditic; whether the same forces are responsible for hermaphroditism in both groups is unclear. The well-established drivers of hermaphroditism in plants (e.g., seed dispersal potential, pollination mode) have analogues in animals (e.g., larval dispersal potential, fertilization mode), allowing us to test the generality of the proposed drivers of hermaphroditism across both groups. Here, we test these theories for 1153 species of marine invertebrates, from three phyla. Species with either internal fertilization, restricted offspring dispersal, or small body sizes are more likely to be hermaphroditic than species that are external fertilizers, planktonic developers, or larger. Plants and animals show different biogeographical patterns, however: animals are less likely to be hermaphroditic at higher latitudes-the opposite to the trend in plants. Overall, our results suggest that similar forces, namely, competition among offspring or gametes, shape the evolution of hermaphroditism across plants and three invertebrate phyla.

Metabolic scaling is the product of life-history optimization.

Organisms use energy to grow and reproduce, so the processes of energy metabolism and biological production should be tightly bound. On the basis of this tenet, we developed and tested a new theory that predicts the relationships among three fundamental aspects of life: metabolic rate, growth, and reproduction. We show that the optimization of these processes yields the observed allometries of metazoan life, particularly metabolic scaling. We conclude that metabolism, growth, and reproduction are inextricably linked; that together they determine fitness; and, in contrast to longstanding dogma, that no single component drives another. Our model predicts that anthropogenic change will cause animals to evolve decreased scaling exponents of metabolism, increased growth rates, and reduced lifetime reproductive outputs, with worrying consequences for the replenishment of future populations.

Relationship between capillaries, mitochondria and maximum power of the heart: a meta-study from shrew to elephant.

This meta-study uses phylogenetic scaling models across more than 30 species, spanning five orders of magnitude in body mass, to show that cardiac capillary numerical density and mitochondrial volume density decrease with body mass raised to the -0.07 ± 0.03 and -0.04 ± 0.01 exponents, respectively. Thus, while an average 10 g mammal has a cardiac capillary density of approximately 4150 mm-2 and a mitochondrial density of 33%, a 1 t mammal has considerably lower corresponding values of 1850 mm-2 and 21%. These similar scaling trajectories suggest quantitative matching for the primary oxygen supply and oxygen consuming structures of the heart, supporting economic design at the cellular level of the oxygen cascade in this aerobic organ. These scaling trajectories are nonetheless somewhat shallower than the exponent of -0.11 calculated for the maximum external mechanical power of the cardiac tissue, under conditions of heavy exercise, when oxygen flow between capillaries and mitochondria is probably fully exploited. This mismatch, if substantiated, implies a declining external mechanical efficiency of the heart with increasing body mass, whereby larger individuals put more energy in but get less energy out, a scenario with implications for cardiovascular design, aerobic capacity and limits of body size.

Predicting the response of disease vectors to global change: The importance of allometric scaling.

The distribution of disease vectors such as mosquitoes is changing. Climate change, invasions and vector control strategies all alter the distribution and abundance of mosquitoes. When disease vectors undergo a range shift, so do disease burdens. Predicting such shifts is a priority to adequately prepare for disease control. Accurate predictions of distributional changes depend on how factors such as temperature and competition affect mosquito life-history traits, particularly body size and reproduction. Direct estimates of both body size and reproduction in mosquitoes are logistically challenging and time-consuming, so the field has long relied upon linear (isometric) conversions between wing length (a convenient proxy of size) and reproductive output. These linear transformations underlie most models projecting species' distributions and competitive interactions between native and invasive disease vectors. Using a series of meta-analyses, we show that the relationship between wing length and fecundity are nonlinear (hyperallometric) for most mosquito species. We show that whilst most models ignore reproductive hyperallometry (with respect to wing length), doing so introduces systematic biases into estimates of population growth. In particular, failing to account for reproductive hyperallometry overestimates the effects of temperature and underestimates the effects of competition. Assuming isometry also increases the potential to misestimate the efficacy of vector control strategies by underestimating the contribution of larger females in population replenishment. Finally, failing to account for reproductive hyperallometry and variation in body size can lead to qualitative errors via the counter-intuitive effects of Jensen's inequality. For example, if mean sizes decrease, but variance increases, then reproductive outputs may actually increase. We suggest that future disease vector models incorporate hyperallometric relationships to more accurately predict changes in mosquito distribution in response to global change.

Metabolism drives demography in an experimental field test.

Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing "rules" for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory-in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.

The roles of diffusion and convection in ventilation of animal burrows.

The relationship between body mass and the respiratory microenvironment of burrowing animals is examined using artificial burrows containing surrogate animals that simulate O2 consumption by removal of air and simultaneous replacement with N2. Allometric relationships between body mass and burrow radius, nest chamber radius, and O2 consumption rate show that published mathematical predictions of diffusion-mediated gas exchange are adequate to describe the respiratory environments of animals in small blind-ending burrows through porous substrata. Diffusion is sufficient to ventilate burrows containing small mammals weighing less than 340 g, or subterranean nest chambers connected to the surface by one or more tunnels containing mammals weighing less than 30 kg. Outside of these limits, convection prevails and prevents the development of hypoxic conditions, particularly in burrows of mammals weighing more than 1300 g.