White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals

Abstract

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

Variable metabolic scaling breaks the law: from ‘Newtonian’ to ‘Darwinian’ approaches

“…Incisive comparative analyses and controlled experiments, including laboratory and field manipulations of the magnitude of specific RS and RD processes, and artificial selection targeting these specific processes should be especially helpful in determining their relative contribution to metabolic scaling relationships under different conditions [8,29,101,102]. An extraordinarily difficult challenge will be to assess the effects of various factors on the scaling of metabolic rate measured under natural, highly variable field conditions, rather than under artificially controlled conditions in the laboratory, as is usually done [144]. Other useful recommendations for further research can be found in [144].…”

“…Furthermore, although traditional theory focusing on the surface law or 3/4-power law has emphasized how physical and geometric constraints on RS and (or) waste removal may cause b to be 2/3 or 3/4 (figure 5b,c), recently many investigators have identified body size-dependent variation in RD by various vital biological structures and processes (e.g. growth, reproduction, locomotion and thermoregulation) as a major cause of variation in b (figure 5d [8,13,25,29,30,43,46,52,53,57,69,[72][73][74]77,101,129,130,144,146]). A RD-centred view has four major advantages over a RS-centred view of metabolic scaling.…”

“…In a scientific sense, investigators studying metabolic scaling are increasingly appreciating ‘diversity and inclusion’ by showing more awareness of the empirical diversity of metabolic scaling patterns, as well as more inclusiveness about the kinds of theory used to explain this diversity. For 25 years, RTN theory that has focused primarily on an ideal, non-existent 3/4-power law has dominated the metabolic scaling field, but many investigators are now invoking multiple mechanisms to explain the diversity of metabolic scaling that actually exists [13,29,30,52,53,98,144]. General theory need not be based on a single primary deterministic mechanism, but may include multiple mechanisms that act in a context-dependent way [13,30].…”

“…New multi-faceted Darwinian approaches focused on adaptable phenotypic plasticity and evolvability show much promise for increasing an understanding of the diversity of metabolic scaling. Recommendations for further research on little-understood topics include studies examining (i) how biological regulatory systems at the molecular, cellular and organismal levels control the phenotypic plasticity of metabolic scaling [13,27,53,77,90,98,148]; (ii) the quantitative genetic basis for the evolvability of metabolic scaling relationships [38,77], including genetically based estimates of b [103]; (iii) relationships between the (co)variation of metabolic rate and body mass and various estimates of evolutionary fitness associated with growth, reproduction and survival [38,53,129,152]; (iv) phylogenetic studies of the evolution of b in relation to diverse intrinsic and extrinsic factors [67,[104][105][106]; (v) the mechanisms causing microevolution of b within conspecific populations, and macroevolution of b across species, including, in particular, multi-variate selection on metabolic rate, body mass and other related traits [38,103,144]; (vi) the effects of various physical, developmental or evolutionary constraints on the boundary limits of b [8,25,29,60,69,82,147]; and (vii) interactive effects of RS and RD processes on metabolic scaling, and how they are influenced directly and indirectly by various interactive biological and ecological factors [13,29,[86][87][88]148]. In short, holistic system analyses involving both proximate (functional) and ultimate (evolutionary) causal fact...…”

“…For example, the ‘metabolic-level boundaries hypothesis’ (MLBH) posits that the metabolic scaling exponent ( b ) depends on the overall metabolic level of an organism (as estimated by the vertical elevation of a metabolic scaling relationship), which in turn depends on activity level, temperature and other biological and ecological factors in diverse taxa for both intra- and interspecific relationships [8,25,56,65,69,72,73,78,87]. This hypothesis and other kinds of ‘contextual multi-modal theory’ include multiple whole-body size-related mechanisms involving surface and internal transport fluxes of metabolic resources and wastes (including heat), the RD of various biological processes and (or) the proportional masses of tissues with different metabolic demands, among other possible mechanisms at the biochemical and cellular levels, whose relative effects on metabolic scaling appear to vary with context [13,29,30,52,53,78,144].…”