Anatomic and Molecular Correlates of Divergent Selection for Basal Metabolic Rate in Laboratory Mice

Abstract

Proximal mechanisms describing the evolution of high levels of basal metabolic rate (BMR) in endotherms are one of the most intriguing problems of evolutionary physiology. Because BMR mostly reflects metabolic activity of internal organs, evolutionary increase in BMR could have been realized by an increase in relative organ size and/or mass-specific cellular metabolic rate. According to the "membrane pacemaker" theory of metabolism, the latter is mediated by an increase in the average number of double bonds (unsaturation index) in cell membrane fatty acids. To test this, we investigated the effect of divergent artificial selection for body-mass-corrected BMR on the mass of internal organs and the fatty acid composition of cell membranes in laboratory mice (Mus musculus). Mice from the high-BMR line had considerably larger liver, kidneys, heart, and intestines. In contrast, the unsaturation index of liver cell membranes was significantly higher in low-BMR mice, mainly because of the significantly higher content of highly polyunsaturated 22 : 6 docosahexanoic fatty acid. Thus, divergent selection for BMR did not affect fatty acyl composition of liver and kidney phospholipids in the direction predicted by the membrane pacemaker theory. We conclude that an intraspecific increase in BMR may rapidly evolve mainly as a result of the changes in size of internal organs, without simultaneous increase of the unsaturation index in cell membrane lipids.

Setting the pace of life: membrane composition of flight muscle varies with metabolic rate of hovering orchid bees

“…Our results illustrate a recurring conundrum in similar studies, such as in experimental evolution studies [28] or studies controlling for body mass and phylogeny [26] that seldom find strong support for the pacemaker hypothesis. Nonetheless, we did find a direct relationship between FlightMR and the abundance of the saturated FA 16 : 0, after controlling for body mass and phylogeny (figure 5).…”

“…Here, insects were used to examine the relationship between membrane composition and metabolic rate, and we report evidence of such a pattern outside the chordates. The resulting implications for the pacemaker hypothesis could be important if strong support can be demonstrated across phyla, because recent research questions its validity [26,[28][29][30]. Furthermore, we test the pacemaker hypothesis using an intermediate phylogenetic scale (within the orchid bee tribe, Euglossini).…”

“…After correcting for the effects of body mass and phylogeny, no significant correlation remains between BMR and any membrane parameter, including unsaturation, % polyunsaturated FAs and % DHA. Similarly, several studies that report intraspecific experiments fail to support the theory [27][28][29]. Mice selected for high BMR over 20 generations decrease their relative abundance of membrane DHA [28], and natural variation in the BMR of mice is positively correlated with % palmitate (16 : 0, a saturated FA) [27].…”

Small organ size contributes to the slow pace of life in tropical birds

“…Metabolic intensity of tissues may vary because of differences in mitochondria (Else and Hulbert, 1985;Moyes, 2003;Porter, 2001;Suarez, 1996), concentrations of metabolic enzymes (Garrido et al, 1996;Marsh and Dawson, 1982;Vézina and Williams, 2005;Weber and Piersma, 1996), activity of the membrane sodium pump (Wu et al, 2001) and fatty acid composition of cell membranes (Brzek et al, 2007;Hulbert and Else, 2005). Variation in BMR between lowland tropical birds and their temperate counterparts could arise if the relative size of some or all of the central organs in tropical species were smaller .…”

Context-dependent correlation between resting metabolic rate and daily energy expenditure in wild chipmunks

“…An inherent, positive coupling between DEE and BMR may occur either centrally, because an increase in the size of energetically expensive digestive organs is required to process more Individual (co)variation in metabolism food (Brzęk et al, 2007;Daan et al, 1990;Konarzewski and Diamond, 1995;Selman et al, 2001), or peripherally, if the tissues at the site of energy use reach maximal capacity, which may also require high maintenance costs such as mammary glands (Hammond et al, 1994). However, recent theoretical and empirical work has suggested that DEE should not be limited to a fixed ratio of BMR.…”