The Evolution of Energetic Scaling across the Vertebrate Tree of Life

Abstract

Metabolism is the link between ecology and physiology-it dictates the flow of energy through individuals and across trophic levels. Much of the predictive power of metabolic theories of ecology derives from the scaling relationship between organismal size and metabolic rate. There is growing evidence that this scaling relationship is not universal, but we have little knowledge of how it has evolved over macroevolutionary time. Here we develop a novel phylogenetic comparative method to investigate how often and in which clades the macroevolutionary dynamics of the metabolic scaling have changed. We find strong evidence that the metabolic scaling relationship has shifted multiple times across the vertebrate phylogeny. However, shifts are rare and otherwise strongly constrained. Importantly, both the estimated slope and intercept values vary widely across regimes, with slopes that spanned across theoretically predicted values such as 2/3 or 3/4. We further tested whether traits such as ecto-/endothermy, genome size, and quadratic curvature with body mass (i.e., energetic constraints at extreme body sizes) could explain the observed pattern of shifts. Though these factors help explain some of the variation in scaling parameters, much of the remaining variation remains elusive. Our results lay the groundwork for further exploration of the evolutionary and ecological drivers of major transitions in metabolic strategy and for harnessing this information to improve macroecological predictions.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…Nevertheless, the rediscovery of nonlinear (curvilinear) metabolic scaling has stimulated a search for additional examples, not only for resting metabolic rate [33], but also for field metabolic rate [34,35] and other biological traits in various taxa [36][37][38]. Why nonlinear interspecific metabolic scaling occurs is unknown, but several hypotheses have been proposed (e.g., [22,[25][26][27][28][29][33][34][35][39][40][41][42][43][44][45][46]). Interestingly, nonlinear metabolic scaling appears to be rare for interspecific analyses [34,43,44], but quite common for intraspecific, ontogenetic analyses (e.g., [19,[47][48][49]).…”

“…Why nonlinear interspecific metabolic scaling occurs is unknown, but several hypotheses have been proposed (e.g., [22,[25][26][27][28][29][33][34][35][39][40][41][42][43][44][45][46]). Interestingly, nonlinear metabolic scaling appears to be rare for interspecific analyses [34,43,44], but quite common for intraspecific, ontogenetic analyses (e.g., [19,[47][48][49]). Nonlinear ontogenetic metabolic scaling relates to developmental changes in energetically demanding processes, such as growth, locomotion and thermoregulation (reviewed in [19,20]).…”

Local adaptation reduces the metabolic cost of environmental warming

“…), particularly among divergent phylogenetic taxa (Uyeda et al. ). Variation in metabolic scaling parameters across and within some species has been linked to consumer body form and temperature (Killen et al.…”

A Bayesian extension of phylogenetic generalized least squares: Incorporating uncertainty in the comparative study of trait relationships and evolutionary rates

“…; Packard and Boardman ; Uyeda et al. ). Also, the dependency of ratematrix on BM is relaxed here by estimating the degree of phylogenetic relatedness (λ) and implementing a MM that can contrasts BM with other alternatives.…”