What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Abstract

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because selfmaintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the 'maintenance costs' of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.Keywords: standard metabolic rate; resting metabolic rate; basal metabolic rate; maternal effects; metabolism; energetics INTRODUCTIONThe energy cost of self-maintenance (when measured as minimal rates of energy metabolism) varies remarkably within species. It effectively forms a central component of life-history theory which concerns how individuals must allocate a finite-energy budget among the competing interests of growth, reproduction and self-maintenance [1]. Compulsory trade-offs among these functions mean that variation in the rate of using energy will probably have implications for life-history traits and hence fitness. Consequently, there is great contemporary interest in amongindividual variation in minimal rates of energy metabolism. In this review, we address two issues: (i) why do some individuals consistently have two or three times the maintenance costs of conspecifics of the same size, age and sex; and (ii) what are the consequences for fitness? For our purposes, the 'baseline' measures of energy metabolism-basal, standard and resting metabolic rate (BMR, SMR and RMR, respectively) are most relevant. When measured on quiescent individuals, at a common temperature and corrected for body mass, these estimate the compulsory energy cost of self-maintenance that is central to life-history theory. The definitions of each vary slightly. SMR is the lowest rate of metabolism, measured at a

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

“…However, they may also benefit from a lower production of reactive oxygen species (ROS; Salin et al 2015b). Such a physiological trade-off between ATP and ROS may help explain the persistence of variation in metabolic rates among individuals; metabolic phenotypes can have differential effects on fitness (Burton et al 2011;Salin et al 2015a). For example, we have shown that individual brown trout with relatively higher SMR perform worse under conditions of low food availability, which may be explained by a reduced capacity to generate ATP above baseline energetic needs (Auer et al 2015c).…”

“…Therefore, AS may have a significant impact on fitness but displays significant intraspecific variation (Farrell et al 2008;Sandblom et al 2014;Auer et al 2015aAuer et al , 2015c; but see Norin et al 2014). Both minimum and maximum metabolic rate are responsible for intraspecific variation in AS since they exhibit consistent differences among individuals over extended periods of time, even within a population under standardized conditions Burton et al 2011;Swanson et al 2012;Careau et al 2014aCareau et al , 2014bGifford et al 2014). In turn, the use of a single metric such as AS conceals a great deal of variation, since individuals with the same AS can have markedly different absolute levels of minimum and maximum metabolic rate (Auer et al 2015c).…”

Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter SnakeThamnophis elegans

“…The low metabolic rate of M-slow snakes at 207C may represent a mechanism to conserve energy when temperatures are low and resources are unavailable (Aleksiuk 1971(Aleksiuk , 1976Burton et al 2011). A low metabolism would allow Figure 2.…”

“…Laboratory studies controlling for resource availability have found both negative (e.g., Danzmann et al 1987) and positive (e.g., Hoogenboom et al 2012) relationships between growth and metabolic rate (reviewed in Glazier 2015). Taken together, these studies indicate that a single optimal metabolic rate may not exist and that fluctuations in resource availability may maintain metabolic polymorphisms within populations (Burton et al 2011;Reid et al 2011).…”

“…In turn, trade-offs in energetic allocation among growth, reproduction, and maintenance compose the basis for life-history theory (Roff 1992;Stearns 1992). Despite decades of empirical and theoretical work, we still lack comprehensive models of the intrinsic and extrinsic drivers of variation in metabolic rate, including the influences of biophysical constraints, ecological heterogeneity, and natural selection (Burton et al 2011;Reid et al 2011;White and Kearney 2013). Even the effects of the three primary determinants of metabolic rate-body size, temperature, and ecological factors-remain unclear and at times debated (Gillooly et al 2001;Agutter and Wheatley 2004;White et al 2006).…”