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

Abstract

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question. INTRODUCTIONEnergy metabolism is one of the most fundamental aspects of biology, and it is key to understanding life histories of living organisms. Its central importance is reflected in the thousands of studies published on energy metabolism (Houston et al., 1993;Hayes and O'Connor, 1999;Speakman, 2008; Burton et al., 2011, Konarzewski andKsiążek, 2013;White and Kearney, 2013). Despite these studies, many questions about metabolic rates and energy metabolism remain unanswered. 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

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

“…However, even if BMR were increased in that study, interpretation of the result would be unclear, because V O 2 swim was measured at 258C and resulted in hypothermia (about 78C [38]), so the selected trait certainly comprised a large component of thermogenesis. Finally, a recent report showed no significant increase in BMR after eight generations of selection for high maximum forced-running V O 2 , even though quantitative genetic analyses performed within the framework of the same experiment showed that both of the traits are heritable and genetically correlated [17]. The lack of change in BMR in this case could simply be due to premature termination of this selection experiment.…”

“…According to the 'aerobic capacity model'-one of the main hypotheses-high BMR in endotherms evolved as a correlated response to selection for increased locomotor performance fuelled by aerobic metabolism [18]. Testing the basic assumption of the model-that BMR is positively correlated with aerobic capacity (maximum rate of oxygen consumption)-has been a motivation for many comparative, experimental, quantitative genetic and conceptual studies, but the issue is not resolved (recent reviews: [13,17,19,20]). …”

“…Benefits of endothermy, which allows maintaining a high body temperature by means of metabolic heat production, are easy to identify. However, evolution of the high level of BMR in birds and mammals, which translates to at least an order of magnitude higher costs of maintenance in comparison to ectothermic reptiles, is puzzling and the selection mechanisms that have led to evolution of such an energetically wasteful strategy remain subject to a vivid discussion (reviews: [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17]). According to the 'aerobic capacity model'-one of the main hypotheses-high BMR in endotherms evolved as a correlated response to selection for increased locomotor performance fuelled by aerobic metabolism [18].…”

Genetic approaches in comparative and evolutionary physiology

“…At the other end of the continuum lie laboratory-based artificial selection experiments, many of which have been conducted with rodents (156,187,211). Some of the examples we find most compelling involve replicated selection at the levels of behavior or whole animal physiological performance.…”

“…Selection experiments are an excellent way to probe the interrelations among traits, including complex traits, because one can atomize an organism to the desired level, impose selection at that level on a trait of interest, and observe correlated cross-generational changes in other traits (58,60,66,187). They are a good way to test specific hypotheses about putative trade-offs (61) and constraints on the way organisms can evolve (e.g., 205,206,211). In particular, they can be a powerful way to demonstrate mechanism, i.e., how organisms work (58,60).…”