Energy assimilation, parental care and the evolution of endothermy

Koteja, Paweł

doi:10.1098/rspb.2000.1025

Cited by 166 publications

(175 citation statements)

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“…An assumption of the aerobic capacity model is that basal metabolic rate (BMR) and MMR are inescapably correlated in endotherms (Hayes and Garland, 1995). Another model that postulates endothermy evolved as a correlated response to selection is the assimilation capacity model (Koteja, 2000). That model suggests that selection acted on the energy assimilation capacity of the visceral organs (for example, liver and gut) and that the assimilation capacity of the visceral organs is correlated with resting metabolic rate.…”

Section: Introductionmentioning

confidence: 99%

“…These models have been questioned because the proposed benefits of initial increases in heat production could be outweighed by elevated energy requirements and would not result in heat production that was rapid enough to enable endothermy (Bennett and Ruben, 1979;Ricklefs et al, 1996;Stevenson, 1985;Angilletta and Sears, 2003). Another set of models suggests that endothermy evolved as a correlated response to selection on genetically correlated characters (Bennett and Ruben, 1979;Ruben, 1995;Farmer, 2000;Koteja, 2000). Perhaps the first of these models was the aerobic capacity model, which postulates that endothermy evolved as a correlated response to selection on maximal metabolic rate (MMR or aerobic capacity) during exercise (Bennett and Ruben, 1979).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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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

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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“…Initially, the issue of the slope of the relationship between BMR and body mass dominated the field, and the discussion continues (McNab 1988;Kozłowski & Weiner 1997;Garland & Ives 2000;Hochachka et al 2003;White & Seymour 2003). Later, the focus shifted to interspecific variation and correlations with life history, environment, food habits and phylogenetic history (McNab 1980;Harvey et al 1991;Koteja & Weiner 1993;Degen et al 1998;Lovegrove 2003), and to the relationship between BMR and maximum or daily metabolic rate (Bennett & Ruben 1979;Koteja 1987Koteja , 2000Hinds & Rice-Warner 1992;Sparti 1992;Hayes & Garland 1995;Ricklefs et al 1996;Degen et al 1998).…”

Section: Introductionmentioning

confidence: 99%

Individual variation and repeatability of basal metabolism in the bank vole,Clethrionomys glareolus

Labocha

Sadowska

Baliga

et al. 2004

Proc. R. Soc. Lond. B

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Basal metabolic rate (BMR) is a fundamental energetic trait and has been measured in hundreds of birds and mammals. Nevertheless, little is known about the consistency of the population-average BMR or its repeatability at the level of individual variation. Here, we report that average mass-independent BMR did not differ between two generations of bank voles or between two trials separated by one month. Individual differences in BMR were highly repeatable across the one month interval: the coefficient of intraclass correlation was 0.70 for absolute log-transformed values and 0.56 for mass-independent values. Thus, BMR can be a meaningful measure of an individual physiological characteristic and can be used to test hypotheses concerning relationships between BMR and other traits. On the other hand, mass-independent BMR did not differ significantly across families, and the coefficient of intraclass correlation for full sibs did not differ from zero, which suggests that heritability of BMR in voles is not high.

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“…The second hypothesis was that a higher BMR may be related to a higher sustained metabolic rate (SusMR); the maximal rate of metabolism that an individual could sustain over days and weeks (Drent and Daan, 1980). This may also provide a context for the evolution of endothermy (Farmer, 2000;Koteja, 2000). SusMR is presumed to be limited by an animal's morphology.…”

Section: Introductionmentioning

confidence: 99%

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

Johnston¹,

Souter²,

Erwin³

et al. 2007

Journal of Experimental Biology

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SUMMARY Basal metabolic rate (BMR) is highly variable, both between and within species. One hypothesis is that this variation may be linked to the capacity for sustained rate of energy expenditure, leading to associations between high BMR and performance during energy-demanding periods of life history, such as reproduction. However, despite the attractive nature of this hypothesis,previous studies have failed to show an association between BMR and fecundity. Our approach was to mate 304 C57BL/6J mice and allow them to wean pups before measuring BMR by indirect calorimetry. We did not find an association between BMR and litter mass, size or pup mass at birth or weaning that could not be accounted for by the body mass of the dam. There was also no relationship between BMR (or BMR corrected for body mass) and birth or weaning success,losses during weaning, or sex ratio. However, a significant relationship was found between BMR and gestational weight loss indicative of foetal resorption. This suggests that during pregnancy the available energy may be limited and partitioned away from the growing foetus and towards maintenance of the mother. In this context, a high BMR may actually be disadvantageous,conflicting with the idea that high BMR may bring reproductive benefits.

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Energy assimilation, parental care and the evolution of endothermy

Cited by 166 publications

References 41 publications

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

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

Individual variation and repeatability of basal metabolism in the bank vole,Clethrionomys glareolus

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

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