Abstract

Summary Variation in aerobic capacity has far reaching consequences for the physiology, ecology, and evolution of vertebrates. Whether at rest or active, animals are constrained to operate within the energetic bounds determined by their minimum (minMR) and sustained or maximum metabolic rates (upperMR). MinMR and upperMR can differ considerably among individuals and species but are often presumed to be mechanistically linked to one another. Specifically, minMR is thought to reflect the idling cost of the machinery needed to support upperMR. However, previous analyses based on limited datasets have come to conflicting conclusions regarding the generality and strength of their association.Here we conduct the first comprehensive assessment of their relationship, based on a large number of published estimates of both the intra‐specific (n = 176) and inter‐specific (n = 41) phenotypic correlations between minMR and upperMR, estimated as either exercise‐induced maximum metabolic rate (VO 2max), cold‐induced summit metabolic rate (Msum), or daily energy expenditure (DEE).Our meta‐analysis shows that there is a general positive association between minMR and upperMR that is shared among vertebrate taxonomic classes. However, there was stronger evidence for intra‐specific correlations between minMR and Msum and between minMR and DEE than there was for a correlation between minMR and VO 2max across different taxa. As expected, inter‐specific correlation estimates were consistently higher than intra‐specific estimates across all traits and vertebrate classes.An interesting exception to this general trend was observed in mammals, which contrast with birds and exhibit no correlation between minMR and Msum. We speculate that this is due to the evolution and recruitment of brown fat as a thermogenic tissue, which illustrates how some species and lineages might circumvent this seemingly general association.We conclude that, in spite of some variability across taxa and traits, the contention that minMR and upperMR are positively correlated generally holds true both within and across vertebrate species. Ecological and comparative studies should therefore take into consideration the possibility that variation in any one of these traits might partly reflect correlated responses to selection on other metabolic parameters. A lay summary is available for this article.

Highlights

  • Metabolism is the ‘fire of life’ that fuels processes at all levels of biological organization (Kleiber 1961) and has far reaching consequences for the physiology, behaviour, in both laboratory (Ksiazz_ek, Konarzewski & Łapo 2004; Wone et al 2015) and wild populations (Boratynski & Koteja 2010)

  • Our meta-analysis shows that there is a general positive association between minMR and upperMR that is shared among vertebrate taxonomic classes

  • The baseline energetic costs of living are set by minMR (Hulbert & Else 2004), which have been quantified as standard metabolic rate (SMR) in ectotherms, basal metabolic rate (BMR) in endotherms, or resting metabolic rate (RMR) as a proxy for the previous estimates under less restrictive conditions

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Summary

Introduction

Metabolism is the ‘fire of life’ that fuels processes at all levels of biological organization (Kleiber 1961) and has far reaching consequences for the physiology, behaviour, in both laboratory (Ksiazz_ek, Konarzewski & Łapo 2004; Wone et al 2015) and wild populations (Boratynski & Koteja 2010). Metabolic rates are often under selection (Hayes & O’Connor 1999; Bochdansky et al 2005) and their variation among individuals has been linked to components of fitness such as growth (Steyermark 2002; Auer et al 2015b), reproduction (Blackmer et al 2005; Boratynski & Koteja 2010) and survival (Artacho & Nespolo 2009; Larivee et al 2010). The links between the lower and upper limits to energy expenditure (minMR and upperMR hereafter) have garnered significant interest over the last half century. UpperMR sets the limit for the energy available to finance locomotion, digestion, growth, reproduction, and thermoregulation. UpperMR has been quantified acutely as maximum metabolism during strenuous exercise (VO2max) or cold-exposure for endothermic organisms (summit metabolism or Msum) and, over longer time spans, as sustained metabolic rates and daily energy expenditure (DEE). Observations that minMR appears to be a relatively constant proportion of both sustained and maximum metabolic rates

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