The origin and maintenance of metabolic allometry in animals

Abstract

Organisms vary widely in size from microbes weighing 0.1 picograms to trees weighing thousands of megagrams, a 10 21-fold range similar to the difference in mass between an elephant and the Earth. Mass has a pervasive influence on biological processes but the effect is usually non-proportional; for example, a 10-fold increase in mass is typically accompanied by just a 4-to-7-fold increase in metabolic rate. Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns. We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds, and mammals. We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

“…Unfortunately, models aimed at explaining scaling exponents notoriously mix intraspecific and interspecific levels by assuming implicitly that the scaling and its relevance to evolutionary processes are identical on both levels. This implicit assumption, which is by no means granted, results from considering body mass as an independent variable rather than a trait evolving in concert with metabolic levels as indicated by White et al (2019). As shown by Kozłowski & Weiner (1997) via life-history modelling, the coevolution of body size and MR may cause the interspecific mass scaling of MR to be shallower than an average intraspecific scaling (Fig.…”

“…This quest has been futile, as illustrated by a recent sequence of papers on basal metabolic rate (BMR) scaling in mammals: White & Seymour (2003) argued for a slope of 2/3, then Savage et al (2004) argued for 3/4, followed by White, Blackburn, & Seymour (2009), Sieg et al (2009) and Capellini, Venditti, & Barton (2010) arguing that neither value was appropriate [see Griebeler & Werner (2016) for review of other papers questioning the universal scaling exponent]. Recently, White et al (2019) used phylogenetic evidence to show that body mass and MR did not evolve independently but were subjected to correlational selection. Understanding the mechanisms of multivariate selection shaping body mass and MR requires a life-history approach that considers a relevant fitness measure.…”

Energetic constraints on mammalian home‐range size

“…Large species maintain large home ranges (body mass–home‐range correlation; Tucker, Ord, & Rogers, ). However, larger species require more energy and endure higher absolute self‐maintenance costs and energy expenditure than smaller species (body mass‐metabolic rate correlations; White et al, ). Consequently, it was hypothesized that it is the rate of metabolic processes that constrain the size of home ranges (Figure a; metabolic rates home‐range size correlations; Mace & Harvey, ; McNab, ).…”

From zygote to a multicellular soma: body size affects optimal growth strategies under cancer risk

“…Multicellularity allows an organism to divide tasks between cells, creating a complex soma with a much wider range of functions than single-celled organisms can achieve (Grosberg and Strathmann, 2007;Knoll, 2011). It also permits large body size, which may help in predator avoidance (Boraas et al, 1998;Kapsetaki and West, 2019) and be subject to other types of selection to become large, including metabolic scaling (White et al, 2019) and intraspecific competition (Kingsolver and Pfennig, 2004;Pettersen et al, 2015). However, creating and maintaining the soma of a multicellular organism is not a trivial task.…”