Genetic Correlations Between Basal and Maximum Metabolic Rates in a Wild Rodent: Consequences for Evolution of Endothermy

Abstract

According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim- and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (= maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.

Associations between basal metabolic rate and reproductive performance in C57BL/6J mice

“…Since we have previously determined the repeatability of this trait in our measurement protocols at around 8% (Krol et al, 2003), only a minor proportion of the total variation we observed can be attributed to random error. This variability in domesticated mice is typically larger, and the corresponding relationships between BMR and body mass poorer, than is observed in other small wild rodents (Koteja, 1995;Sadowska et al, 2005). This probably reflects the high variability in the contribution of metabolically inert body components such as adipose tissue to the variance in body mass of domestic mice.…”

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

“…A number of studies have suggested that BMR would likely show a correlated response to direct selection on MMR (Koteja, 1987;Bozinovic, 1992;Dohm et al, 2001;Rezende et al, 2004;Nesoplo et al, 2005a;Sadowska et al, 2005;Wone et al, 2009). Likewise many evolutionary models suggest complex interrelationships among traits linked to metabolic rates (Ricklefs and Wikelski, 2002;Downs et al, 2013).…”

“…In a population of bank voles (Clethrionomys glareolus) with a positive genetic correlation between BMR and MMR (Sadowska et al, 2005), selection for increased MMR was accompanied by a correlated increase in BMR (Sadowska et al, 2008).…”

“…For example, is there a universal metabolic scaling law, why is resting metabolism correlated with daily energy use in mammals but not birds, how did the diverse resting and maximal metabolic rates of animals evolve and is there a necessary correlation between resting and maximal aerobic metabolism in vertebrates (Ricklefs et al, 1996;Clavijo-Baque and Bozinovic, 2012)? Some of these questions are very difficult to answer but ecological and evolutionary physiologists have recently made increasing use of artificial selection experiments to test hypotheses about the phenotypic and genetic integration of energy metabolism (Swallow et al, 1998;Koch and Britton, 2001;Ksiażek et al, 2004;Rezende et al, 2004;Sadowska et al, 2005Sadowska et al, , 2008Swallow et al, 2009;Wone et al, 2009;Gebczyński and Konarzewski 2009a, b,). One of the foci of these recent studies has been testing hypotheses about the evolution of endothermy.…”

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species

“…Although intra-and inter-specific associations between RMR and MMR have been studied extensively in endothermic lineages (Dutenhoffer and Swanson 1996;Hinds and RiceWarner 1992;Koteja 1991;Rezende et al 2004;Rezende et al 2002;Sadowska et al 2005;Wone et al 2009), much less is known about how these metabolic rates are related in ectothermic species (but Taigen 1983, Walton 1993, Thompson and Withers 1997. More extensive analyses are needed to determine the generality of relationships between RMR and MMR and their morphological, physiological, behavioural and ecological correlates across diverse ectothermic groups.…”