Metabolic rate and environmental productivity: Well-provisioned animals evolved to run and idle fast

Abstract

Even among vertebrate species of the same body mass and higherlevel taxonomic group, metabolic rates exhibit substantial differences, for which diverse explanatory factors-such as dietary energy content, latitude, altitude, temperature, and rainfall-have been postulated. A unifying underlying factor could be food availability, in turn controlled by net primary productivity (NPP) of the animal's natural environment. We tested this possibility by studying five North American species of Peromyscus mice, all of them similar in diet (generalist omnivores) and in gut morphology but differing by factors of up to 13 in NPP of their habitat of origin. We maintained breeding colonies of all five species in the laboratory under identical conditions and consuming identical diets. Basal metabolic rate (BMR) and daily ad libitum food intake both increased with NPP, which explained 88% and 90% of their variances, respectively. High-metabolism mouse species from high-NPP environments were behaviorally more active than were lowmetabolism species from low-NPP environments. Intestinal glucose uptake capacity also increased with NPP (and with BMR and food intake), because species of high-NPP environments had larger small intestines and higher uptake rates. For metabolic rates of our five species, the driving environmental variable is environmental productivity itself (and hence food availability), rather than temporal variability of productivity. Thus, species that have evolved in the presence of abundant food run their metabolism ''fast,'' both while active and while idling, as compared with species of less productive environments, even when all species are given access to unlimited food.M etabolic rate means the rate at which an animal burns calories to produce energy. Among vertebrate species, there is a 10 7 -fold range of metabolic rates. Much research has aimed at understanding the reasons behind this variation. Why are some animals seemingly extravagant, consuming and expending calories rapidly, whereas others are frugal, consuming very little and metering their expenditure accordingly so as to remain in energy balance?The two factors underlying most of this variation are well known: body mass and higher-level taxonomic affiliation. First, within the same higher-level taxonomic group (e.g., mammals), metabolic rate increases with body mass (the so-called mouseto-elephant curve) according to approximately the 0.75 power of body mass (1). (Metabolic rate per g of body mass decreases with body mass but by a power smaller than 1.0, so the absolute metabolic rate of a whole animal, the subject of this paper, increases with mass). Second, for species of the same mass there are some differences between higher-level taxonomic groups, notably the ca. 8-fold difference between endotherms (''warmblooded'' birds and mammals) and ectotherms (''cold-blooded'' reptiles, amphibia, and fish) (2), and also the ca. 1.3-fold difference between marsupials and placentals (3) and the ca. 2-fold difference between sloths and other placentals (4).Ho...

Reduction of Energetic Demands through Modification of Body Size and Routine Metabolic Rates in Extremophile Fish

“…Notably, extremophiles have consistent reductions in body size in natural habitats that drive an overall reduction of energy demands. Hence, environmentally induced changes in energy supply and demand may be a major diving force in metabolic rate evolution (Mueller and Diamond 2001).…”

“…Resource availability is a strong source of selection driving adaptive modification of metabolic rates within and among closely related species (Mueller and Diamond 2001;McCue 2010;Moiroux et al 2012). From an energetic point of view, fitness can be described as the conversion rate of energy into offspring (Brown et al 1993), which ultimately is limited first by the rate at which organisms can acquire energy from the environment and then by the rate at which they can allocate energy to reproduction (as opposed to maintenance or growth).…”

Analysis of the effects of inbreeding on lifespan and starvation resistance in Drosophila melanogaster

“…Whether good quality individuals have higher or lower rate of metabolism is however still an unresolved question (Hawkins and Day 1999;Konarzewski and Diamond 1995;Reinhold 1999;Nilsson 2002;Rantala and Roff 2006;Johnston et al 2007;Ketola and Kotiaho 2009a, b;Mikkelsen et al 2010). The environment in which a population has evolved to live may have fundamental effects on its metabolic strategy in the sense that a low metabolic rate is favored in areas where food supply is scarce, while high metabolic rate is favored in areas where food supplies are abundant (Mueller and Diamond 2001). Experiments on laboratory populations that have been reared on abundant food for several generations may therefore be conducted on high energy consuming individuals adapted to ample food conditions.…”

Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes

“…Consequently, short-lived species could have increased metabolic rates if they live in productive environments facilitating large investment in reproduction. Mueller & Diamond (2001) recently showed that this could indeed be the case as metabolic rate of Peromyscus mice species increases along a habitat gradient that differs 12 times in net primary productivity. However, there are many other environmental factors apart from productivity and predictability that can potentially influence the pace of life, such as predation risk (Ghalambor & Martin 2001) and food availability (Ricklefs 1991;Martin 1995).…”