Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function

Downs, Cynthia J.; Brown, Jessi L.; Wone, Bernard; Donovan, Edward R.; Hunter, Kenneth W.; Hayes, Jack P.

doi:10.1098/rspb.2012.2636

Cited by 40 publications

(40 citation statements)

References 81 publications

(123 reference statements)

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“…Likewise many evolutionary models suggest complex interrelationships among traits linked to metabolic rates (Ricklefs and Wikelski, 2002;Downs et al, 2013). Although the selection for high MMR might possibly have led to high BMR in the evolutionary past, our results are equivocal with respect to the importance of a genetic covariance constraining the evolution of metabolic rates in the mice we studied.…”

Section: Discussioncontrasting

confidence: 55%

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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: Discussioncontrasting

confidence: 55%

“…The breeding scheme was previously described (Downs et al, 2013), but is described here with additional detail. As mentioned previously, metabolic rates correlate strongly with mass.…”

Section: Study Organismmentioning

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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“…This is one of various examples in which predictions about trade-offs derived from basic physiological principles are not necessarily met in practice, perhaps because nature has more 'degrees of freedom' than expected (e.g. Garland, 1988;Downs et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Finally, HR mice have evolved increased maximal oxygen consumption (V · O2max ), as measured during forced treadmill exercise (Rezende et al, 2009), and another selection experiment with laboratory house mice that targeted V · O2max found evidence for altered innate immune function (e.g. decreased cytokine production in response to a lipopolysaccharide injection) in their selected lines (Downs et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Immune response to aTrichinella spiralisinfection in house mice from lines selectively bred for high voluntary wheel running

Dlugosz

Schutz

Meek

et al. 2013

Journal of Experimental Biology

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SUMMARYFour lines of mice bred for high voluntary wheel running (HR lines) have high baseline circulating corticosterone levels and increased daily energy expenditure as compared with four non-selected control (C) lines. High corticosterone may suppress immune function and competing energy demands may limit ability to mount an immune response. We hypothesized that HR mice have a reduced immune response and therefore a decreased ability to fight an infection by Trichinella spiralis, an ecologically relevant nematode common in mammals. Infections have an acute, intestinal phase while the nematode is migrating, reproducing and traveling throughout the bloodstream, followed by a chronic phase with larvae encysted in muscles. Adult males (generation 55 of the selection experiment) were sham-infected or infected by oral gavage with ~300 J1 T. spiralis larvae. During the chronic phase of infection, mice were given wheel access for 6 days, followed by 2 days of maximum aerobic performance trials. Two weeks post-infection, infected HR had significantly lower circulating immunoglobulin E levels compared with infected C mice. However, we found no statistical difference between infected HR and C mice in numbers of encysted larvae within the diaphragm. As expected, both voluntary running and maximum aerobic performance were significantly higher in HR mice and lower in infected mice, with no line type-by-infection interactions. Results complement those of previous studies suggesting decreased locomotor abilities during the chronic phase of T. spiralis infection. However, despite reduced antibody production, breeding for high voluntary wheel exercise does not appear to have a substantial negative impact on general humoral function. Supplementary material available online at

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“…An immune response, in turn, is a costly mechanism mediated through metabolic trade-offs [2][3][4] and/or hormonal signalling that may not be directly related to energy expenditures [5][6][7]. Surprisingly, the associations between immunocompetence, energy expenditure and survival have not been extensively studied and are typically researched separately.…”

Section: Introductionmentioning

confidence: 99%

Immunocompetence and high metabolic rates enhance overwinter survival in the root vole, Microtus oeconomus

et al. 2014

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Despite its presumed significance, the association between immune defence, energy expenditures and overwinter survival is rarely studied. We analysed individual variation in immunocompetence quantified as neutrophil-tolymphocyte ratio (N/L), total white blood cells (WBC) and natural antibody levels, along with resting (RMR) and peak metabolic rates (PMR) and mortality during three consecutive winter seasons in a natural population of the root vole, Microtus oeconomus. In early winter, WBC count was negatively correlated with RMR, whereas N/L ratio was negatively correlated with swim-elicited PMR. We suggest that while the first correlation reflected the trade-off between energy allocation in immunocompetence and other metabolically demanding processes, the latter correlation stemmed from stress-induced immunosuppression elicited by the necessity to cope with swimming in frequently flooded habitat. In addition, the analysis carried out during the first year of study characterized by a high population density and prevalence of infestation with a blood parasite-Babesia spp., showed that its intensity was inversely correlated with the N/L ratio. In summary, our results suggest that elevated N/L ratio increases the winter survival of free-ranging rodents by increasing their ability to cope with parasitic infections.

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Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function

Cited by 40 publications

References 81 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

Immune response to aTrichinella spiralisinfection in house mice from lines selectively bred for high voluntary wheel running

Immunocompetence and high metabolic rates enhance overwinter survival in the root vole, Microtus oeconomus

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