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

Abstract

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 (h 2 ) 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 (ϭ 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. Birds and mammals employ an extravagant economy of energy usage. They spend energy at a rate about 20 times higher than do reptiles (Nagy et al. 1999) and dissipate 20-50% of the energy as basal metabolism for maintenance of basic function (McNab 2002). How such a wasteful strategy of energy use evolved from an energetically frugal strategy is puzzling. This puzzle is the core of a nearly half-centurylong debate on selection forces behind the evolution of endothermy (i.e., the ability to maintain an elevated body temperature by means of metabolic heat production) in birds and mammals (see reviews: Hayes and Garland 1995;Ruben 1995;Farmer 2000Farmer , 2003 Koteja 2000Koteja , 2004McNab 2002;Angilletta and Sears 2003;Gomes et al. 2004).Although several hypotheses concerning the evolution of endothermy have been proposed, only one-the aerobic capacity model-has been subject to extensive empirical testing. According to the model, high basal metabolic rate (BMR) and consequently endothermic thermoregulation, evolved as a correlated response to selection for an ability of sustained locomotor activity, supported by aerobic metabolism (Bennett and Ruben 1979), rather than as a response to direct selection for thermoregulatory capability. A fundamental assumption of the hypothesis is that the aerobic capacity is functionally linked with BMR, which translates into a statistically tractable hypothesis of a positive correlation between BMR and the maximum rate of oxygen consumption (V O2max ), and therefore can be tested against empirical results obtained in extant species. The assumption has been...

Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment

“…-Results of the current selection experiment, taken together with results of our previous quantitative genetic analyses [32], provide 'steady' support for the assumption that selection for increased aerobic capacity should lead to increased BMR. However, the results also indicate that it is unlikely that such a selection alone could result in the roughly 10-fold difference in BMR between endotherms and ectotherms.…”

“…In our previous work [32], we reported a positive genetic correlation between V O 2 swim and BMR. However, the voles in our previous study swam at 308C and therefore V O 2 swim also comprised a thermoregulatory burden.…”

“…In this paper, we present a comparison of the level of BMR of voles from lines selected for 11 generations with that of unselected, control lines (C). Based on results from our earlier quantitative genetic analyses, we predicted that BMR will increase both in lines selected for high swim-induced aerobic metabolism [32] and in lines selected for herbivorous capability [33]. Because of a close connection between predatory propensity and locomotor activity, shown also in other selection experiments [45], and in line with the aerobic capacity model of the evolution of endothermy [16,46], we predicted that BMR will also increase in lines selected for increased predatory behaviour.…”

“…[30][31][32][33][34]) and selection experiments [2,[35][36][37][38][39][40][41] have been recognized as powerful tools in such studies (but see [19,20,42,43] for discussion of limitations of these tools).…”

Tropical birds have a slow pace of life

“…Our assertion that natural selection is responsible for differences in metabolism between these two groups requires that BMR is heritable, an idea with some support (67)(68)(69). Life-history theory suggests that lower extrinsic mortality in the tropics results in a suite of changes in reproductive variables among species that live there, generally described as low reproductive effort (70)(71)(72), and that adults allocate more energy to self-maintenance (73), thereby increasing survival rate.…”