Positive allometry of sexually selected traits: Do metabolic maintenance costs play an important role?

Sexual selection drives the evolution of some of the most exaggerated traits in nature. Studies on sexual selection often focus on the size of these traits relative to body size, but few focus on energetic maintenance costs of the tissues that compose them, and the ways in which these costs vary with body size. The relationships between energy use and body size have consequences that may allow large individuals to invest disproportionally more in sexually selected structures, or lead to the reduced per-gram maintenance cost of enlarged structures. Although sexually selected traits can incur energetic maintenance costs, these costs are not universally high; they are dependent on the relative mass and metabolic activity of tissues associated with them. Energetic costs of maintenance may play a pervasive yet little-explored role in shaping the relative scaling of sexually selected traits across diverse taxa. Also see the video abstract here: https://youtu.be/JyuoQIeA33Q.

Metabolic theory predicts animal self-thinning.

The metabolic theory of ecology (MTE) predicts observed patterns in ecology based on metabolic rates of individuals. The theory is influential but also criticized for a lack of firm empirical evidence confirming MTE's quantitative predictions of processes, e.g. outcome of competition, at population or community level. Self-thinning is a well-known population level phenomenon among plants, but a much less studied phenomenon in animal populations and no consensus exists on what a universal thinning slope for animal populations might be, or if it exists. The goal of this study was to use animal self-thinning as a tool to test population-level predictions from MTE, by analysing (i) if self-thinning can be induced in populations of house crickets (Acheta domesticus) and (ii) if the resulting thinning trajectories can be predicted from metabolic theory, using estimates of the species-specific metabolic rate of A. domesticus. I performed a laboratory study where the growth of A. domesticus was followed, from hatching until emergence as adults, in 71 cohorts of five different starting densities. Ninety-six per cent of all cohorts in the three highest starting densities showed evidence of self-thinning, with estimated thinning slopes in general being remarkably close to that expected under metabolic constraints: A cross-sectional analysis of all data showing evidence of self-thinning produced an ordinary least square (OLS) slope of -1·11, exactly that predicted from specific metabolic allometry of A. domesticus. This result is furthermore supported by longitudinal analyses, allowing for independent responses within cohorts, producing a mean OLS slope across cohorts of -1·13 and a fixed effect linear mixed effects models slope of -1·09. Sensitivity analysis showed that these results are robust to how the criterion for on-going self-thinning was defined. Finally, also as predicted by metabolic theory, temperature had a negative effect on the thinning intercept, producing an estimate of the activation energy identical to that suggested by MTE. This study demonstrates a direct link between the metabolic rate of individuals and a population-level ecological process and as such provides strong support for research that aims to integrate body mass, via its effect on metabolism, consumption and competition, into models of populations and communities.

Relationship between growth and standard metabolic rate: measurement artefacts and implications for habitat use and life-history adaptation in salmonids.

Mass-specific standard metabolic rate (SMR, or maintenance metabolism) varies greatly among individuals. Metabolism is particularly sensitive to variation in food consumption and growth creating the potential for significant bias in measured SMR for animals that are growing (e.g. juveniles) or of uncertain nutritional status. Consequently, interpreting individual variation in metabolism requires a sound understanding of the potentially confounding role of growth and the relative importance of fixed (genetic) vs. environmental drivers of SMR variation. We review the role of growth in measured SMR variation in juvenile salmonids, with the goals of (i) understanding the contribution of growth (and food consumption) to SMR variation through ontogeny, (ii) understanding the relative contributions of tissue maintenance and biosynthesis (overhead costs of growth) to apparent SMR variation, and (iii) using intrinsic growth effects on SMR to model how alternate life-history strategies may influence growth and measured SMR in juvenile salmonids. SMR measures on juveniles, even when post-absorptive, may be inflated by delayed growth-associated overhead costs, unless juveniles are on a maintenance ration (i.e. not growing). Empirical measurements of apparent SMR in food restricted vs. satiated 2-5 g juvenile salmon demonstrate that estimates may be inflated by as much as 67% due to delayed overhead costs of growth, even when SMR measurements are taken 35 h post-feeding. These results indicate that a substantial component of variation in apparent SMR among juvenile salmonids may be associated with (i) environmentally driven variation in ration (where elevated SMR measurements are an artefact of delayed growth overhead costs), (ii) intrinsic (genetic) or plastic organ-system trade-offs related to increasing investment in metabolically expensive digestive tissue responsible for processing food and (iii) intrinsic (genetic) variation in maximum body size and growth among individuals or life-history types. We suggest that selection for differences in adult body size among resident and anadromous forms leading to differences in juvenile growth trajectories may contribute to both SMR variation and habitat segregation in freshwater, where juveniles with higher growth are constrained to foraging in high velocity habitats to meet their greater consumption needs.

Size matters: plasticity in metabolic scaling shows body-size may modulate responses to climate change.

Variability in metabolic scaling in animals, the relationship between metabolic rate ( R: ) and body mass ( M: ), has been a source of debate and controversy for decades. R: is proportional to MB: , the precise value of B: much debated, but historically considered equal in all organisms. Recent metabolic theory, however, predicts B: to vary among species with ecology and metabolic level, and may also vary within species under different abiotic conditions. Under climate change, most species will experience increased temperatures, and marine organisms will experience the additional stressor of decreased seawater pH ('ocean acidification'). Responses to these environmental changes are modulated by myriad species-specific factors. Body-size is a fundamental biological parameter, but its modulating role is relatively unexplored. Here, we show that changes to metabolic scaling reveal asymmetric responses to stressors across body-size ranges; B: is systematically decreased under increasing temperature in three grazing molluscs, indicating smaller individuals were more responsive to warming. Larger individuals were, however, more responsive to reduced seawater pH in low temperatures. These alterations to the allometry of metabolism highlight abiotic control of metabolic scaling, and indicate that responses to climate warming and ocean acidification may be modulated by body-size.

Discontinuous, biphasic, ontogenetic shifts in the metabolic allometry of aquatic animals?

Several investigations in recent years have reported patterns of discontinuous, biphasic, loglinear variation in the metabolic allometry of aquatic animals. These putative shifts in pattern of allometry have been attributed to changes in the primary site for gas exchange from cutaneous to branchial as animals undergo ontogenetic changes in size, shape, and surface area. Because of the important implications of the earlier research with regard to both physiology and evolution, I re-examined data that purportedly support claims of discontinuous, biphasic allometry in oxygen consumption versus body size of American eels (Anguilla rostrata) and spiny lobsters (Sagmariasus verreauxi). I used ANCOVA to fit three different statistical models to each set of logarithmic transformations and then assessed the fits by Akaike's Information Criterion. The observations for both species were described better by a single straight line fitted to the full distribution than by a biphasic model. Eels, lobsters, and other aquatic animals undergo changes in shape and surface area as they grow, but such changes are not necessarily accompanied by changes in the pattern of metabolic allometry.

What is complex allometry?

Complex allometry describes a smooth, curvilinear relationship between logarithmic transformations of a biological variable and a corresponding measure for body size when the observations are displayed on a bivariate graph with linear scaling. The curvature in such a display is commonly captured by fitting a quadratic equation to the distribution; and the quadratic term is typically interpreted, in turn, to mean that the mathematically equivalent equation for describing the arithmetic distribution is a two-parameter power equation with an exponent that changes with body size. A power equation with an exponent that is itself a function of body size is virtually uninterpretable, yet numerous attempts have been made in recent years to incorporate such an exponent into theoretical models for the evolution of form and function in both plants and animals. However, the curvature that is described by a quadratic equation fitted to logarithms usually means that an explicit, non-zero intercept is required in the power equation describing the untransformed distribution - not that the exponent in the power equation varies with body size. Misperceptions that commonly accompany reports of complex allometry can be avoided by using nonlinear regression to examine untransformed data.

Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans.

Studies of how a mammal's daily energy expenditure scales with its body mass suggest that humans, whether Westerners, agro-pastoralists, or hunter-gatherers, all have much lower energy expenditures for their body mass than other mammals. However, non-human primates also differ from other mammals in several life history traits suggestive of low energy use. Judging by field metabolic rates of free-ranging strepsirhine and haplorhine primates with different lifestyle and body mass, estimated using doubly labeled water, primates have lower energy expenditure than other similar-sized eutherian mammals. Daily energy expenditure in humans fell along the regression line of non-human primates. The results suggest that thrifty energy use could be an ancient strategy of primates. Although physical activity is a major component of energy balance, our results suggest a need to revise the basis for establishing norms of energy expenditure in modern humans.